17.1 Introduction: Thinking About Terminology

This chapter will focus on the other half of the urogenital system—the reproductive part. As we alluded to in Chapter 16, these are tied together through the occasional co-opting of various ducts initially associated with the kidneys. Before we start our conversation about reproduction, it is worth pausing and considering the language that we use. In this case, we are not talking about the many colorful turns of phrase that people use to refer to their reproductive parts but rather discussing sex and gender.

If you were to briefly and randomly survey scientific papers across time that study animal reproduction, mating behavior, or any similar thing, you would see the terms “sex” and “gender” used interchangeably, regardless of the animal, for much of that history. In the last several years, there has been a shift in terminology, and more studies use “sex” when studying nonhumans. The current general definition of sex is that it is a classification based on the structural and functional characteristics of an organism, and there are several more specific definitions of sex that focus on particular characteristics. These could be chromosomes, the presence or absence of particular reproductive organs, or hormone levels, for example (there are plenty more characteristics that could be used). In humans, sex is often assigned at birth on the basis of external genitalia. Often the categories of sex used for a particular species (including humans) are binary, male or female. However, when it comes to nonvertebrate organisms, there are other systems. We use + or – for some green algae. The unicellular ciliate Tetrahymena thermophile has seven sexes, and they are numbered with Roman numerals (I–VII). Relying on a binary classification system also tends to ignore the many organisms (including vertebrates) that are hermaphroditic (possessing both “male” and “female” genitalia at some point in their lives, whether that is simultaneous or sequential). For humans, we instead use the term intersex to refer to people who are born with genital or gonad anatomy or chromosomal patterns that do not fit into the binary boxes of “male” and “female.”

Gender is a human social construct that denotes identities such as woman, man, agender, nonbinary, two-spirited, and more. Because gender is an identity and a social construct, it is human-specific. Nonhuman animals have a sex, but not a gender.

We also want to remind our readers that the human spectrum is diverse, as is the variation we see within many other species. In humans, sex and gender intersect in complex ways. To honor that, we are going to use “egg producer” or “ovary-bearing” and “sperm producer” or “testis-bearing” instead of “female” and “male,” respectively, as not all egg producers are “female,” and not all sperm producers are “male.”

17.2 Structure and Function of the Reproductive System

At its most basic, reproductive systems generally consist of gonads (which are responsible for making gametes), some sort of genital duct (a path for the gametes to travel through), and some sort of opening for gametes (or other reproduction-related things) to enter or exit the body. There is an incredible amount of variability across sexes, species, and higher taxonomic levels (Figure 17.1). Variation is tied to lifestyle (e.g., aquatic vs. terrestrial), fertilization behavior (external vs. internal), parental care, and evolutionary history, among other things. We will begin by describing some of the general components of the vertebrate reproductive system here, and then we will save our discussion of the fascinating variation of these systems for after we’ve talked about development.

Components of the Egg-Producer Reproductive Systems

Ovaries are the gonads that produce eggs, or ova (singular: ovum). This is not the ovary’s only job, as it is also an active component of the endocrine system (see Chapter 21 for a discussion of endocrine function). However, the production and maturation of ova (oogenesis) are closely tied to the endocrine function of the ovary as a gland. The general structure of the vertebrate ovary can best be described as a bundle of follicles held together with some connective tissue (Figure 17.2). These follicles are composed of two things—oocytes and follicle cells. Follicle cells form a layer around the oocytes and help provide the yolk within the developing ovum. Oocytes (literally, “egg cells”) can be thought of as precursors to mature ova (see Section 17.3, Morphological Development). The follicles and associated connective tissue are enclosed by a capsule of connective tissue called the tunica albuginea, which is overlaid by a layer of epithelium. The ovary is suspended from the coelom wall by a ligament called the mesovarium (mesos = middle, ovo = egg; Figure 17.3). You may recall that we saw similar sheets of suspensory tissue called mesenteries in the digestive system (Chapter 13), and the similarity in name is no accident.

When ova are released from an ovary, a process called ovulation, the eggs are shed into the coelom (Figure 17.1). In the vast majority of vertebrates, the oviduct is close by and collects the eggs. The oviduct is also referred to as the Müllerian duct, which we will talk about when we get to development. The oviduct can include a wide variety of structures, depending on which vertebrate you’re examining, including the uterus, vagina, cervix, and shell glands. Not all vertebrates have all these regions of specialization.

While you may assume that the ovaries and oviducts are paired structures as they are in many humans, this is not the case in several vertebrates. Almost every vertebrate class has species that have only one functional ovary or oviduct; this can be due to the fusion of gonads, the atrophy of one gonad or oviduct, or the failure of one gonad to develop at all. Birds, in particular, tend to only have a left functional ovary, while the right ovary atrophies while the bird is still an embryo.

Components of Sperm-Producer Reproductive Systems

Testes (singular: testis) are the gonads that produce sperm, a process called spermatogenesis. Similar to ovaries, testes also have an endocrine function (see Chapter 21). In fact, we’re going to see a lot of parallels in structure as well! Recall that the ovaries are generally made up of connective tissue and follicles. Similarly, the testes are made up of somatic tissue and seminiferous tubules, the former of which includes connective tissue, nerves, blood vessels, and Leydig cells (Figure 17.4). Leydig cells (also known as interstitial cells) are responsible for producing androgen hormones. Spermatogenesis takes place within the seminiferous tubules. Sertoli cells, a major structural component of the seminiferous tubules, are in contact with the germ cells and aid the production of sperm (see Section 17.3, Morphological Development). The seminiferous tubules merge together into collecting ducts, which then meet up with the ductus deferens. For most vertebrates, the testes are internal and suspended from the coelom wall by a ligament called the mesorchium (literally, “middle testicle” in Greek). Mammals are the exception; many mammals instead have external testes contained within a pouch called the scrotum. The migration of the testes from within the coelom to an external position will be discussed later in this chapter. The testes are covered by an epithelium, and beneath that is a layer of connective tissue called the tunica albuginea, just as we saw in the ovaries. Also as we saw with ovaries, testes are not always paired; they can be completely fused into one testis, they can be partially fused, or just one testis may develop fully.

Unlike eggs, sperm are generally not released into the coelom. Instead, for most vertebrates, the archinephric duct (opisthonephric duct) from the renal system is co-opted for sperm transport (Figure 17.1). In some vertebrates, this duct may carry urine and sperm (although not simultaneously), but recall from the previous chapter that amniotes instead rely on a metanephric duct for urine transport. As we saw with the oviduct, the archinephric duct may include regional specializations, depending on which vertebrate you’re examining.

Sperm-producing vertebrates may also possess intromittent organs, which are external organs that help transmit sperm in internal fertilizing species. In mammals, this is known as the penis, and we will see other intromittent organs when we dive into the diversity of reproductive systems.

17.3 Morphological Development

Regardless of whether a vertebrate develops gonads capable of making ova or sperm, the gonads arise from the genital ridge, specifically as mesoderm with contributions from the mesenchyme. At this initial stage, the paired masses of tissue do not show any particular sperm- or egg-related features; as such we call it an indifferent gonad (Figure 17.5). The germ cells that eventually will make gametes originate outside of the genital ridge in the extraembryonic endoderm. Once the germ cells arrive at the indifferent gonad, we start to see some differentiation. For many vertebrates, germ cells will migrate to the cortex of the indifferent gonad if the gonad will be producing eggs, but they will migrate to the medulla of the gonad if the gonad will be producing sperm. However, cyclostomes and teleosts do not follow this pattern, and germ cells migrate to the cortex regardless of what the gonad develops into.

When germ cells reach the ovary, we change their name to oogonia. These oogonia go through several steps during oogenesis. Briefly, the oogonia carry two complete sets of chromosomes, making them diploid. They divide via mitosis, and those products of cell division are called primary oocytes (Figure 17.6). The primary oocytes then proceed through Meiosis I, producing a small polar body and a larger secondary oocyte. If you remember your meiosis, these are haploid. During Meiosis II, we split the sister chromatids between two cells so that a haploid ovum is created from the secondary oocyte, along with another small polar body (also haploid). The haploid polar body produced by Meiosis I may or may not go through Meiosis II. It’s worth noting that the process of oogenesis is extremely variable across vertebrates in terms of developmental timing and sometimes is not completed until the end of reproductive maturity or even until fertilization takes place.

Spermatogenesis is a process that is similar to oogenesis (Figure 17.7). When germ cells reach the testes and the Sertoli cells, we change their name to spermatogonia. Like the oogonia, they are diploid. As these develop during spermatogenesis, they undergo rounds of mitosis, and those products are called primary spermatocytes. Those diploid cells will undergo meiosis, forming haploid secondary spermatocytes at the end of Meiosis I and spermatids after Meiosis II. Unlike oogenesis, no polar bodies are formed during this process. Instead, we make four haploid spermatids. Spermatids undergo a final step where the chromosomes are condensed and excess cytoplasm and organelles are removed from the cell. When this is complete, we have sperm (or more properly, spermatozoa).

To sum up all of this, both eggs and sperm are produced via meiosis. However, the products differ. One diploid oogonium will produce a single egg that can be fertilized and two to three polar bodies that will not. One diploid spermatogonium will produce four sperm that can potentially fertilize an egg.

The processes governing whether a vertebrate ends up with ovaries or testes (sex determination) are complex and variable. As one might expect, there is often a genetic component. We call this genetic sex determination (GSD). At the chromosome level, many vertebrates have some sort of chromosomes that are tied particularly to sex determination. In mammals and some lizards, we see X and Y chromosomes, where the XX condition (homogamous, because we see the same chromosomes) is usually associated with egg producers, and XY (heterogamous) is associated with sperm producers. However, in birds, some lizards, and snakes, we see Z and W chromosomes and the opposite condition, where the ZZ homogamous condition is associated with sperm producers, and the ZW heterogamous condition is associated with egg producers. Amphibians and fishes can be either XY or ZW, depending on the species. Interestingly, the XY chromosomes are not homologous to the ZW chromosomes, and they act in very different ways. For example, the mammalian Y chromosome contains a gene called Sry, which is not found on the X chromosome. Sry is the gene that causes the indifferent gonad to develop into a testis by stabilizing the SOX9 protein, which in turn jump-starts the development of both Sertoli cells and testicular cords. The absence of Sry expression causes the indifferent gonad to develop into an ovary. It’s worth noting that there is a whole series of gene expression and inhibition events that are required to move forward with gonadal development that is beyond the scope of this chapter, and there are genes other than Sry in nonmammalian vertebrates that perform similar functions. There are resources at the end of this chapter if you are interested in learning more.

Genes are not the sole determinant of sex in some vertebrates. There are several vertebrates that rely on environmental sex determination. Some reptiles, such as the tuatara, crocodylians, and many turtles do not have sex chromosomes. Instead, they have temperature-dependent sex determination (TSD). High versus low incubation temperature is not firmly tied to sex across all TSD species. Many turtle hatchlings tend to be ovary-bearing if they are incubated at high temperatures, whereas high-temperature incubation tends to lead to crocodilian hatchlings developing testes instead of ovaries. In still other reptiles, such as the loggerhead sea turtle, there is a more complex TSD regime, where both high and very low incubation temperatures produce hatchlings with ovaries, and more intermediate temperatures produce hatchlings with testes. How exactly TSD works with respect to temperature affecting gene expression is an active area of research with no clear answers yet.

Another form of environmental sex determination uses social cues. Roughly 450 teleost species are sequential hermaphrodites, meaning that they transition between functional ovaries and functional testes (or vice versa) at some point in their lives (Figure 17.8). Most are protogynous, initially possessing functional ovaries. Wrasses, which include parrotfish, are wonderful examples. Bluehead wrasse, which can be found on reefs throughout the Caribbean, have initial GSD; most start off bearing ovaries, but a small number will have testes. In this initial phase, both sexes have similar yellow, green, and white coloration. Initial-phase wrasses participate in group spawning, gathering in large groups, and releasing gametes into the water. A small number of initial-phase bluehead wrasses will transition from ovary-bearing to testis-bearing. When this happens, the initial ovaries redifferentiate into testes, followed by the body changing color to include the bright-blue heads that give these fish their common name. Interestingly, these terminal-phase testis-bearers also change their spawning behavior, only mating in pairs. The social cue that initiates these changes is a decrease in the number of large sperm-producing wrasses in the population, and transition happens within two weeks.

A smaller percentage of hermaphroditic fishes are protoandrous, and my favorite example is the clownfish of Finding Nemo fame. This Indo-Pacific reef fish tends to live in groups consisting of one breeding pair (the largest fish has functional ovaries and the next largest has functional testes), plus up to four smaller nonbreeding fish. These fish start their lives with both testicular and ovarian tissues, and as they mature, only the testicular tissue becomes functional. If the largest ovary-bearing fish dies or is removed from the group, the second largest fish will transition from having functional testes to having functional ovaries—the testicular tissue regresses and the ovarian tissue matures. If you’re thinking back to the beginning of Finding Nemo when (spoiler alert!) Marlin’s mate dies…yes, Marlin should have transitioned.

An even smaller percentage of teleosts, mostly a few coral-dwelling goby species and the cleaner wrasse Labroides dimidatus, can engage in serial bidirectional sex change. This is a relatively recent discovery, and most of the species identified were previously assumed to be protogynous. Some of the gobies can repeatedly switch back and forth, which is thought to be an adaptation to limited mating opportunities on coral reef heads that are fairly isolated. Generally, these gobies have ovotestes, with a portion of the gonad being composed of ovarian tissue and the other portion composed of testicular tissue. Keeping this gonad bisexual allows the gobies to switch sexes more rapidly.

The development of the genital ducts has been partially covered already in the previous chapter. Recall that the archinephric ducts have been co-opted for sperm transport; the development of these ducts has been discussed in Chapter 16. However, we haven’t talked about the Müllerian ducts yet. For the vertebrates that have them at some point in development, these ducts form from mesonephric epithelial tissue surrounded by mesenchyme and more epithelium. As the embryo develops, most vertebrates that develop testes lose the Müllerian ducts; in mammals, this is thanks to the production of anti-Müllerian hormone (AMH) by the testes.

17.4 Reproductive System Evolution and Diversity

With the exception of the cyclostomes, we are going to follow the evolution of the sperm-producing vertebrates first. We will then circle back and discuss the evolution of the ovary-bearing vertebrates. This will let us first follow a trend that we saw in the previous chapter (the co-opting of the archinephric duct to carry sperm), and then we can focus on the many evolutionary changes that ovary-bearing vertebrates accrued as they became more terrestrial (egg-laying is ancestral, as is external fertilization). This means that we will be covering each group of vertebrates twice (except cyclostomes). As a reminder, there is a basic schematic of these reproductive systems in Figure 17.1.

Cyclostomes

Lampreys and hagfishes have relatively simple reproductive systems. They have gonads and that’s about it—there are no genital ducts at all (Figure 17.1). Instead, the ovaries and testes shed their gametes directly into the coelom (Figure 17.9). Gametes leave the body by moving through the coelom and through genital pores, which develop only after these fishes reach reproductive maturity. The gametes pass through the pores into the urinary sinus and then leave the body through an opening called the cloaca (Latin for “sewer” or “drain”). Lampreys and hagfishes are external fertilizers, meaning that they shed their gametes into the water. It’s worth noting that this relatively simple reproductive system is not limited to our jawless friends. There are several basal actinopterygians—such as tarpons, moray eels, and arowanas—that utilize genital pores instead of genital ducts.

Remember that when we introduced ovaries, we noted that these are not always paired. Hagfishes only have the right ovary, as the left one degenerates. Lampreys also have only one ovary, but this is a case of fusion—the right and left primordia fuse early in development, resulting in a single ovary located on the midline. Similarly, lampreys and hagfishes have single testes.

Testes-Bearing Gnathostomes

Chondrichthyans

Sperm is produced in paired testes, located at the anterior end of the coelom (Figures 17.11 and 17.12). Sperm pass into a series of ducts called the efferent ducts (also known as vasa efferentia and ductus efferens); these are derived from the nephric tubules.

For each testis, the efferent ducts serving it merge into a single duct called the vas deferens, which is also known as the opisthonephric duct, the ductus deferens, or the Wolffian duct (see Table 17.1 for all the duct names). The vas deferens does not carry urine in the chondrichthyans—remember from the previous chapter that they have accessory urinary ducts to drain the kidneys and pass urine to the ureter. The anterior part of the vas deferens is highly convoluted and referred to as the epididymis. The sperm travel from the epididymis, down the vas deferens, to the enlarged posterior portion called the seminal vesicle or ampulla ductus deferens. Leydig glands contribute seminal fluid at the epididymis and middle portion of the vas deferens; sperm plus seminal fluid is what we call semen. Both the middle portion of the vas deferens and the seminal vesicle can store sperm and seminal fluid. The seminal vesicles empty their contents into a urogenital sinus; the “uro” in the name indicates that this cavity also receives urine from the ureter (though not usually at the same time). Both urine and semen leave the urogenital sinus through projections called urinary papillae (singular: urinary papilla; also known as urogenital papilla) that extend into the cloaca.

Table 17.1—A guide to the different duct names in the urogenital systems of vertebrates

Chondrichthyans are internal fertilizers. That means that the sperm need to find their way inside the ovary-bearing shark, skate, or ray. Sperm-producing chondrichthyans have secondary sex organs (i.e., not gonads and ducts) called claspers and siphon sacs (Figure 17.13). Claspers are modifications of the medial part of the pelvic fins and are composed of several pieces of cartilage that are joined to the metapterygium and one another. Each clasper has a dorsal groove that runs longitudinally down the clasper. During copulation, a single clasper is rotated and inserted into the cloaca of the egg-producing shark. Sperm is ejected from the urinary papilla down the groove, where it can make its way toward the oviduct of the other shark. Sperm gets a boost from the seawater in the siphon sacs, which are internal muscular bladders that open at the proximal opening of the clasper.

Osteichthyan Fishes

Most bony fishes have paired testes that are fairly elongated. However, we also see cases where only one testis develops, partially fused testes (e.g., perch), and completely fused testes (e.g., guppies). Bony fish testes tend to fall into one of two categories: tubular (contains highly branched spermatic tubules within the testis) or lobular (less branched spermatic tubules; Figure 17.14). As you might guess, those tubes contain the Sertoli cells responsible for spermatogenesis, as well as other epithelial cells.

How the sperm leave the testes largely depends on what type of bony fish you’re looking at. Some have no ducts and shed sperm directly into the coelom and utilize genital pores, as we mentioned in the cyclostomes section. Other nonteleost bony fishes (sturgeons, paddlefish, lungfishes) have co-opted the opisthonephric duct, just as we saw in the chondrichthyans. However, unlike the chondrichthyans, their opisthonephric duct still carries urine as well as sperm. In sturgeons, efferent ducts connect the testes to canals within the kidneys. The kidney canals can also carry urine and will carry both urine and sperm to the opisthonephric duct. The connections work differently in the sarcopterygian lungfishes—the efferent ducts connect the testis with the opisthonephric duct, not the kidneys. The paired ducts may or may not merge at the urinary papilla, which empties into the cloaca.

The teleosts do not follow either of these plans (Figure 17.1). The opisthonephric duct is only used to transport urine, not sperm, and we can call it a ureter in this case. Instead, teleosts develop a testicular duct to transport sperm. The testes contain small spermatogenic tubes. The spermatogenic tubes merge as they exit the testes, forming the testicular duct. Note that this means that the testicular duct is not homologous with the opisthonephric duct! The testicular duct passes through the coelom and ends at the point where sperm leave the body. Usually, this takes place through an opening between the anus and the urinary aperture. Other teleost species have testicular ducts that connect with the urethra, and sperm and urine will leave through a urogenital papilla (Figure 17.15).

The majority of bony fishes are external fertilizers and release their gametes into the water in a process called spawning. Spawning can happen in large groups or in pairs, in the open ocean or near the sea floor, and so forth. There is a lot of variation in fish spawning behavior. The timing of spawning is not random! Fishes time their spawning events using cues such as seasonal changes of light, seasonal changes of temperature, and the phase of the moon (as a proxy for tidal movement). Approximately 3% of bony fishes are internal fertilizers, and this strategy has arisen independently at least 12 times in bony fish evolution, including in the coelacanths, rockfishes, and guppies. While 3% may seem small, remember that there are approximately 28,000 osteichthyan species; just within the teleosts, this strategy is spread across 21 families and somewhere between 500 and 600 species! How do they accomplish this? In general, there is some sort of structure that a sperm-producing fish can insert into an egg-producing partner. For example, sperm-producing guppies have developed a gonopodium, long extensions to the third through fifth rays of the anal fin, which functions similarly to claspers in sharks in that it is inserted into the ovary-bearing fish and used to transfer sperm (Figure 17.16). Other fishes, such as rockfishes and surfperch, will insert their urogenital papilla into the reproductive partner.

Amphibians

All amphibians have paired, lobular testes composed of seminiferous tubules, which are the site of spermatogenesis and Sertoli cells, as well as connective tissues, nerves, blood vessels, and Leydig cells. Amphibians also possess a pair of fat bodies, one adjacent to each testis (Figure 17.17). As you might guess, fat bodies are full of lipids. In terms of reproduction, they are capable of synthesizing steroid hormones and thus are important to gamete formation. Sperm travels from the seminiferous tubules to the efferent ducts, as we have seen in other vertebrates. However, unlike other vertebrates, the efferent ducts connect to nephrons within the kidney. In salamanders, this is relegated to only nephrons in the anterior “genital kidney,” as mentioned in Chapter 16. Once sperm leave the kidney, they head into the Wolffian duct to head to the cloaca and exit the body. That means this duct carries both sperm and urine to exit the body in the majority of amphibians. Interestingly, plethodontid salamanders (“lungless” salamanders) are the exception to this rule, as the testes do not connect to the kidney. Thus, the Wolffian duct is solely a sperm-carrying duct until it is close to the cloaca and urinary ducts merge with it.

The gymnophionans (caecilians) have an additional feature—the Müllerian duct remains intact in sperm-producing caecilians and empties into the cloaca. In egg-producing caecilians, this duct is the oviduct, as we would expect. But in our adult sperm producers, this duct functions as a gland, producing a variety of products that mix with sperm in the anterior part of the cloaca to help with sperm motility and physiology. The caecilians are notable for another reason: The cloaca of sperm-producing caecilians can evert itself into the vent (opening) of the ovary-bearing caecilians and thus acts as an intromittent organ during internal fertilization. Specifically, the posterior part of the cloaca called the phallodeum is shaped like a tube. When it’s time to mate, muscles evert the phallodeum; when mating is done, another set of muscles retracts it.

Most salamanders are also internal fertilizers, although this is a very different process than that of the caecilians (Figure 17.18). Sperm-producing salamanders that practice internal fertilization package their sperm in gelatinous masses called spermatophores; these are produced in cloacal glands. Often, they will deposit spermatophores on a substrate, and the ovary-bearing salamander will walk over it and uptake it into their cloaca. Other salamanders will directly place the spermatophore into the other salamander’s cloaca.

Anurans (frogs) are largely external fertilizers, although they do not generally spawn as bony fishes do. Instead, the sperm-producing frog will get on the egg-producing frog’s back and secure themselves by grasping the head, waist, or armpits with their forelimbs. This behavior is called amplexus (Latin for “embrace”; Figure 17.19). As eggs are being extruded by one frog, the other releases sperm directly on top of the eggs. Internal fertilization is rare and seems to only occur in the two species of “tailed frogs” (Ascaphus; Figure 17.20). The common name is misleading, as the “tail” in question is actually an extension of the cloaca in sperm-producing tailed frogs. This part of the cloaca is highly vascularized. When it is time to mate, the tissues become engorged, and the “tail” is inserted into the egg-producing frog. Sperm runs from the cloaca down a groove in the “tail,” much as we saw in shark claspers.

Amniotes

The biggest evolutionary trend we’ve followed throughout this book is the shift from a fully aquatic lifestyle to a fully terrestrial one. In terms of reproduction, we have now seen hints of what this looks like from a reproductive perspective in the amphibians: internal fertilization, the copulatory organs that go along with that, and (preview for the section on egg producers) fewer, larger eggs. All amniotes are internal fertilizers and have some sort of organ for copulation. This is generally called a penis, but we will see that some reptiles have hemipenes, and most extant birds have either greatly reduced or totally lost their penis. We will talk more about these shortly.

Aside from the penis (or hemipenes, or lack thereof), the general layout is the same regardless of which amniote you’re examining (Figures 17.1 and 17.11). Sperm are produced in the paired testes and travel through the efferent ducts, epididymis, and then Wolffian ducts to leave the body. The other major shift that occurs in sperm-producing amniotes is related to the kidney evolution we talked about in the previous chapter—the separation of urine and sperm into different tubes becomes the rule. Recall that our Wolffian ducts are just another word for opisthonephric ducts, and these end up being used entirely for sperm transport in amniotes, whereas a new duct forms (the metanephric duct or ureter) to handle urine transport. Because these Wolffian ducts solely carry sperm, we often refer to them as the vas deferens to distinguish them from Wolffian ducts that carry both sperm and urine.

Reptiles, Including Aves

Testes-bearing reptiles, including birds, generally only differ once you get down to the point where sperm are leaving the body. Turtles and crocodylians have single, unpaired penises that are tucked into the cloaca until it’s time to copulate. However, they work in very different ways. Turtles have two ridges of erectile tissue called seminal ridges that run down the length of the penis. A seminal groove lies between the two ridges. Turtle penises have a single erectile region composed of a corpus fibrosum and the corpus cavernosum (Figure 17.21). As the corpus cavernosum fills with blood, the penis is erected. Once inserted into the other turtle, sperm travels down the seminal groove into the other turtle’s reproductive tract. Turtles have a retractor muscle to pull the penis back into the cloaca, which originates on the sacral ribs and inserts onto the ventral corpus fibrosum. Penis morphology varies quite a bit among turtles. Several species have a sulcus and glans (tip or head of the penis) that bifurcate, or split in two. One genus of soft-shelled turtles, Trionyx, has a five-lobed glans, each lobe with a separate opening for the split urethra.

Crocodylians, on the other hand, do not have erectile tissue in their penises. Paired levator muscles, which originate at the anterior cloaca and insert on the penis, rotate the penis out of the cloaca. This causes strain on a ligament that connects the base of the penis to the ischia, which serves to erect the penis. Crocodylians also have a central groove, called the sulcus spermaticus, for sperm to travel down. When those levator muscles relax, the strain on the ligament eases and the penis returns back into the cloaca.

Squamates (lizards and snakes) do something totally different—they have hemipenes. The paired hemipenes are tucked away just caudal to the cloacal vent when they are not in use (Figures 17.22 and 17.23).

When it’s time to copulate, sperm travels through the Wolffian ducts and exits into the cloaca at the base of the hemipenes. Just one hemipenis is everted straight into the ovary-bearing squamate’s cloacal vent via contraction of the transversus penis muscle (Figures 17.24 and 17.25). Each hemipenis has a sulcus spermaticus for the sperm to travel down from the cloaca. As we saw with the turtles, there is a retractor muscle to pull the hemipenes back into the cloaca. Some varanid (monitor) lizards have some erectile help from a hemibaculum, or hemipenis “bone,” located in the glans of the hemipenis. Note that the hemibaculum is composed of cartilage, not bone tissue. We will see that some mammals have something similar made of bone.

Approximately 3% of extant birds have external(ish) genitalia. Most of the time, they’re tucked away in the cloaca within a pocket, and you don’t see them until postcopulation. This is because, unlike many other amniotes, they are erected with lymph and not blood. As you may recall from Chapter 15, the lymphatic circulation operates at a much lower pressure than the blood circulation. Thus, bird penises are erected into the other bird’s vaginal canal. The most basal living birds, paleognaths (e.g., ostriches, emus, tinamous, and rheas), retain them. Given that we also see penises in crocodylians, this suggests that extinct dinosaurs likely did as well. A few neognaths retain them, particularly ducks and a few other fowl. The shape of these penises is variable, from penises that veer to the left (ostriches, kiwis) to highly coiled penises (ducks, tinamous; Figure 17.26).

So why did birds lose their external genitalia? Like for many other bird features, one of the reigning hypotheses is to lighten the body as much as possible for flight. Yet ducks and other fowl are long-distance migrators. Other hypotheses that show promise include minimizing sexually transmitted infections and preventing unwanted copulation. We will return to this when we get to ovary-bearing birds.

If there is no intromittent organ in most extant birds, how does internal reproduction take place? Copulating birds simply line up their cloacas and sperm is transferred into the other bird’s cloaca. This behavior is called a “cloacal kiss,” as fleshy lips surround each bird’s cloaca (Figure 17.27).

Mammals

So far, we’ve seen that the testes are located cranially in the coelom in most vertebrates. For most terrestrial mammals, the testes are located externally. This shift is called “the descent of the testes” and occurs during development (Figure 17.28). The testes are attached to a ligament in the scrotum. This ligament, called the gubernaculum (this author’s favorite anatomical word, for the record), shortens through development, pulling the testes caudally through the inguinal canal and finally into the scrotum. The gubernaculum persists in anchoring the testes to the scrotum.

There are two main hypotheses for why this change occurred. The first considers temperature control for the developing sperm. Mammals tend to keep their internal body temperature rather high, which may be too high for optimal sperm production. Externally, temperatures are cooler. Some mammals, such as rats and other rodents, can retract their testes and scrotum into their abdominal cavity with the cremaster muscle. This same muscle is used to draw the human scrotum closer to the body. The second hypothesis concerns locomotion, specifically galloping. The muscles activated during galloping can produce large fluctuations in abdominal pressure, which in turn could cause some leaking of sperm, since there are no muscular sphincters to keep semen where it belongs. Interestingly, the majority of galloping mammals have external testes. On the other hand, elephants have internal testes (and do not gallop), as do marine mammals. However, they are still somewhat descended. Elephants retain their testes within the abdominal cavity, whereas marine mammals such as pinnipeds and whales send their testes through the inguinal canal but not into a scrotum. It is unlikely that there is a single, one-size-fits-all answer for all mammals.

After sperm leave the testes (Figure 17.1 for a general schematic), what happens next depends on the mammal in question. Monotremes have a urogenital sinus at the base of the bladder, which receives both urine from ureters (which does eventually end up in the bladder) and sperm from the testes (Figure 17.29). In echidnas, urine leaves the urogenital sinus through the urinary papillae. Semen, on the other hand, leaves through the penis. As such, the penile urethra only carries sperm. Echidna penises have a “rosette glans,” where the glans is split into two sections, and each of those forms a bifurcated structure called a rosette. Each rosette has its own urethral opening and epidermal spines, which means that the urethra splits into four parts as well. When not in use, the penis is stored above the cloaca. Erection causes the penis to pass through a sphincter and then the lumen of the cloaca before exiting. Initially, all four rosettes are erect, but only two of the four rosettes remain erect and ejaculate. Similarly, the platypus has a bifurcated urethra and glans with epidermal spines.

In therians (marsupials and “placental” eutherian mammals), the vas deferens connects to the urethra, which thus carries both sperm and urine (Figure 17.28). The urethra is centrally located within the penis, which is surrounded by erectile tissue—a paired corpora spongiosum and a ventral erectile tissue called the corpus cavernosum. Some mammals, such as walrus, raccoons, ground squirrels, and bears, have further support by a baculum (os penis; Figure 17.30). These shapes range from a simple long rod (bears, sea lions) to spoon shaped (ground squirrels) or trident shaped (rice rats, voles). The external morphology of therian penises is also quite variable.

The surface of the penis may include structures such as keratinous spines, hooks, flaps, and papillae. The location of these structures is also variable across species, whether they’re located on the glans, shaft, or base of the penis. It’s not clear what all these structures are for, although spines have been hypothesized to induce ovulation by stimulating the vaginal tract or to aid in sperm competition. Most eutherians have a single glans and shaft; marsupial penises are bifurcated in some species. The latter has been hypothesized to correspond to the ovary-bearing marsupials that have two vaginal openings (see the Mammals section of Ovary-Bearing Gnathostomes).

Ovary-Bearing Gnathostomes

Chondrichthyans

Sharks and their relatives can have either paired ovaries or a single ovary, with the second ovary either completely absent or underdeveloped. A number of sharks belonging to the Galeomorphii, such as hammerheads and bull sharks, have a fully formed right ovary and an underdeveloped left ovary (Figure 17.31). A small number of rays instead retain the left ovary.

As we will see with many other vertebrates (including us!), the ovaries are not directly connected to the oviducts. Ovulation, the process of an ovum leaving the ovary, instead dumps the ova into the coelom. However, the funnel-shaped opening of the oviduct, the ostium, is right next to the ovary, so the ova are unlikely to go astray. As the oviducts curve away from the ovaries and move posteriorly toward the cloaca, there is an enlarged section in the anterior portion of the oviduct. This is the shell gland (sometimes also referred to as the oviducal gland or nidamental gland). This gland is responsible for secreting an egg capsule or membrane over the ovum after the ova is fertilized; it is also sometimes used for sperm storage after copulation. After an egg (fertilized or not) leaves the shell gland, it enters the uterus, which is just an enlarged section of the oviduct (as it is in us!). Remember that many sharks and their relatives have two functioning ovaries and thus two functioning oviducts. That means there are also two uteruses. In elasmobranchs, the two uteruses will merge posteriorly, which then leads to the cloaca. In holocephalans (chimeras and ratfish), the uteruses do not merge before reaching the cloaca and have separate openings.

Whether the embryonic chondrichthyan develops in the uterus or not depends on the species of chondrichthyan. We see some that are oviparous—such as horn sharks, cat sharks, and many skates—which means they lay eggs and their embryonic development mostly takes place outside of the parent’s body. This is likely the ancestral condition for chondrichthyans, based on some fossilized egg cases from the Devonian period. Other chondrichthyans are viviparous, giving “live birth,” and this can take many different forms (see Box 17.1). No chondrichthyan is known to care for their offspring once they’ve left the parent’s body.

Osteichthyes

As we saw in the sperm-producing Osteichthyes, there is a lot of variation in reproductive anatomy in the bony fishes. When we discussed the cyclostomes, we mentioned that some bony fishes (tarpons, moray eels, and arowanas) do not have oviducts to catch those eggs that are ovulated into the coelom; instead, they utilize genital pores. Ova then enter the urogenital sinus and leave through the cloaca. They tend to have solid ovaries. Most teleosts have hollow ovaries, where ovulation releases ova into ovarian cavities that are connected to an ovarian duct or gonoduct (Figure 17.32). This tube essentially functions as an oviduct does, catching the ovum and sending it on its path toward leaving the body. Therefore, you will still see it called an oviduct in other papers and books. However, the ovarian duct forms from the dorsal visceral peritoneum and peritoneum lining the ovarian cavity and not the mesonephric epithelial tissue. Thus, the teleost ovarian duct is likely not homologous to the oviduct we see in other vertebrates, and we have chosen not to use “oviduct” for this structure to indicate that. Regardless of whether the ovaries are solid or hollow, bony fishes may have paired ovaries with one larger than the other, partially fused ovaries, or fully fused ovaries.

When we look at tetrapods, lungfishes, and coelacanths, we see that their oviducts are indeed true oviducts, derived from that Müllerian duct (Figure 17.33). There are actinopterygians that have true Müllerian ducts—gar, bowfins (Amia), sturgeons, and bichirs all do, which means that some of the Neopterygii (gar, bowfin) have them, while the teleosts (also a subdivision of the Neopterygii) do not. Remember, teleosts are (1) highly derived fishes and (2) not the closest ancestors of the tetrapods. In other words, they have done their own thing when it comes to reproductive anatomy. So where did the gonoducts evolutionarily come from? We don’t know! Scientists have been looking at genetics, histology, and of course, anatomy to try to figure this out. It’s not clear if they are derived from the genital pores, if they are somehow still homologous with the Müllerian duct, or even whether they are derived from the testicular ducts; these are all hypotheses that scientists are currently sorting through.

Recall that the vast majority of bony fishes are external fertilizers; thus they are oviparous. However, unlike the chondrichthyans, there are several species that practice some sort of parental care. This may include behaviors such as hiding eggs, nest guarding, mouth brooding (carrying fertilized eggs in the oral cavity), or something as unusual as the testes-bearing seahorse Hippocampus carrying developing eggs in a ventral brood pouch. The egg-producing seahorses deposit their unfertilized eggs into the brood pouch, which is located ventral to the gonopore. Sperm are released above the pouch and make their way into the brood pouch’s lumen (cavity) to fertilize the eggs. The new zygotes implant in the brood pouch, which triggers the tissues of the pouch to change, including increasing vascularization to help regulate osmolality, gas exchange, and nutrient supplementation.

Box 17.2—What Do We Know About Fossil Fishes?

As we’ve said before, the soft and squishy bits do not fossilize particularly well. So our knowledge of extinct organisms’ organ systems beyond the skeletal system is spotty, at best. However, as we will see when we talk about dinosaur reproduction later in this chapter, we can use both direct and indirect evidence to make some hypotheses about reproduction. While we don’t have anything to help us figure out what was going on with our ancient jawless fishes, there are some fossils that can help us out with the placoderms. For example, there are some placoderm fossils from Latvia and the US that are clearly juveniles and occur in areas that appear to be potential nursery sites. While there haven’t been any egg cases found, the current hypothesis is that these particular placoderms were oviparous. However, other placoderms were internal fertilizers with viviparity. A beautifully preserved placoderm from Australia, aptly named Materpiscis (literally, “mother fish”), was preserved with an embryo (Figures 17.34 and 17.35). Soon after, two other genera were also found with preserved embryos inside their bodies. Further evidence for internal fertilization comes from preserved clasper-like pelvic fins for a few genera of placoderms.

Amphibians

Generally, the anatomy of the egg-producing amphibians is as we would expect: Paired, sac-like ovaries produce ova, which are released into the coelom (Figure 17.36). The ova are picked up by the oviducts, which eventually connect to the cloaca. As we saw in the sperm-producing amphibians, finger-shaped fat bodies lie adjacent to the ovaries and are important for supporting gamete production via the hormones they secrete. The oviducts are divided into three parts:

1. The pars recta, also known as the infundibulum, is where the ova enter the oviduct.
2. The pars convulata, also known as the ampulla, tends to be full of twists and turns. It is responsible for adding the gelatinous layers to ova via oviductal glands and is the longest portion.
3. The pars utera, also known as the uterus or ovisac, is the most posterior part of the oviduct and ends at the cloaca. Ova can be held here until the amphibian is ready to mate. Some amphibians have tubules to store sperm in this portion of the oviduct.

Salamanders can also store spermatophores and fertilized eggs in their cloacal glands.

Terrestrial adults with aquatic breeding habits, which are the likely ancestral mode of life, are oviparous. This includes external fertilizers, like most frogs, which lay their eggs in water and leave them to develop without any parental care. This is probably the most familiar form of amphibian reproduction—eggs are laid in an aquatic environment where larvae (such as tadpoles) hatch and later metamorphose into adults. Aquatic adults tend to only have aquatic breeding habits and follow a similar plan. However, amphibians are not limited to this reproductive strategy! Terrestrial adults with terrestrial breeding habits might be oviparous but do not lay eggs in water. Instead, they may lay fewer, larger eggs to protect against desiccation (Figure 17.37). These amphibians, roughly half of all salamander species and one-third of frog and caecilian species, have no larval stage and just hatch looking like miniadults.

Other terrestrial breeders are viviparous. Viviparous caecilians are particularly interesting. They retain fertilized eggs in pars utera. Once the eggs hatch, the larvae need to eat, and the only food available is the tissue lining the pars utera. While that may be an extreme example of parental care, roughly 75% of the amphibian families have evolved some sort of parental care including nest building, egg tending, and egg brooding in various anatomical parts (including dorsal sacs, vocal sacs, and stomachs). In amphibians with external fertilization, parental care most often comes from the sperm-producing sex. The egg-producing amphibians tend to provide parental care if they use internal fertilization.

Amniotes

Again, we remind you of our big evolutionary trend—the shift from aquatic to terrestrial habitats—and that reproduction also had to change to accommodate that shift. However, one particular major evolutionary innovation helped vertebrates completely divorce themselves from relying on the aquatic realm for reproduction: the amniotic egg (also known as the cleidoic egg; Figure 17.38). This is also one of the synapomorphies for amniotes and the feature that gives amniotes their name.

Fish and amphibian eggs do share some features with amniotic eggs. The parts of the egg that we are interested in are called extraembryonic membranes—“extra” meaning “outside,” so these are things that are not the embryo itself. The yolk sac, which contains the yolk, is an extraembryonic membrane that we see in most vertebrate eggs. Because fish and our ancestral amphibian eggs were laid in water, the embryos could stay hydrated, and gas exchange and waste removal could easily happen in this aqueous medium. However, a move to land meant that eggs could dry out and waste had nowhere to go. A more watertight shell and three new extraembryonic membranes aided this transition to land. The chorion and allantois (Greek for “sausage,” as it looks when it first develops) are both derived from the ectoderm and mesoderm, and in many amniotes, they eventually merge to store waste and participate in gas exchange (sometimes referred to as the chorioallantois). The amnion not only produces amniotic fluid, which helps prevent desiccation, but it also contains contractile fibers that can move the embryos early in development to ensure they do not adhere to any of the extraembryonic membranes. We will revisit these membranes again once we get to ovary-bearing mammals.

We also see another new reproductive feature in the ovary-bearing amniotes, the clitoris (Figure 17.39). This structure is homologous to the penis of testes-bearing amniotes. During development, there are three paired structures. The anterior and posterior cloacal swellings, as the name suggests, give rise to the cloaca. The third structure, the genital tubules, forms either a penis or clitoris; the fate is determined by the relative amounts of testosterone and estrogen. Structurally, the two organs are also similar.

Adult crocodylians and turtles have a well-developed clitoris, and they have corresponding tissue to penises. The clitoris has been studied in some mammals, such as various primates, rodents, and bottlenose dolphins (see Box 16.3 for more!). Just as testis-bearing snakes and lizards have hemipenes, ovary-bearing snakes and lizards have a hemiclitoris. Given the homology between the clitoris and penis and that most extant testes-bearing birds have either a reduced or absent penis, it probably isn’t surprising that a bird clitoris has only been found early in development and not in adults. However, the function of this organ and why it is retained is not well studied. Some hypothesize that it functions primarily for sexual pleasure, which is difficult to study in animals. However, we also know that in some mammals such as rats, cattle, and pigs, stimulation of the clitoris during copulation can lead to increased pregnancy rates. Other hypotheses include that the clitoris serves to increase vaginal lubrication and to prepare the reproductive organs for sperm.

Reptiles, Including Aves

Reptilian oviducts are often divided into five sections: The ovum enters the infundibulum, uterine tube (also known as the magnum in birds, as it’s the largest section of the oviduct), isthmus, uterus (also called a shell gland in birds), and vagina (where the egg will leave the oviduct; Figure 17.40). There is a considerable amount of variation in how well differentiated these five regions are. For example, many squamates (lizards and snakes) have infundibula and uterine tubes that are not particularly different from each other. On the other hand, not only do the extant archosaurs (crocodylians and birds) have well-differentiated sections, but the infundibulum and uterus are further subdivided into anterior and posterior portions that have different functions. While it is clear that the oviduct as a whole is homologous across reptiles, the individual sections may not be.

In turtles, crocodylians, and birds, the uterine tube / magnum is responsible for forming much of the albumen (what we know as “egg whites” in our kitchens). However, albumen-producing glands have not been found in squamate oviducts at all, and squamate eggs don’t contain much of this fluid either. The isthmus is also quite variable across reptiles in terms of what tissues and glands it’s composed of. As such, it’s not clear if this section is homologous across all reptiles. For example, we know that in birds, the inner and outer shell membranes are formed on the egg here. In crocodylians, the anterior portion of the uterus is structurally and functionally similar to the isthmus of birds, producing those membranes. Similarly, the posterior portion of the crocodilian uterus lays down the eggshell, and the section immediately prior to the vagina in birds (often called the shell gland) does the same. These are likely also homologous with each other. There are also sperm storage tubules located at the junction between the vagina and posterior uterus in both birds and crocodylians. Turkeys can store their sperm for up to 10 weeks! Note that crocodylians and birds are all oviparous. We will come back to this.

In squamates and turtles, the uterus does something different. For oviparous squamates (and all turtles are oviparous), all layers of the eggshell including their membranes are formed in the uterus. Viviparity has evolved independently in various squamate groups over 100 times, and uteri of viviparous species have incubation chambers and do not make eggshell material. Note that for all our oviparous reptiles, including birds, fertilization of the ovum has to happen prior to the eggshell being laid down. Viviparous squamates utilize a placenta to feed their embryos, just as many mammals do. However, with the many independent origins of viviparity in squamates, we get six different types of placentas made of different tissues. All squamate placentas are composed of a combination of extraembryonic membranes from the embryo and uterine epithelium from the parent. The variation comes from which extraembryonic membranes are integrated into the placenta. Most often it’s both the chorion and allantois, but some placentas use the yolk sac or other single membranes.

Bird vaginas are wildly diverse in morphology (Figure 17.41). They can be a simple folded tube, or they can be full of spirals with blind pouches. Waterfowl are particularly well studied, as there is a lot of variation in vaginal morphology across different species. It seems that the complexity of vaginal morphology is correlated with the commonality of forced extrapair (outside of a mated partner) copulation within a species as well as penile shape. For example, African geese Anser sygnoides do not practice forced copulation and have short penises; correspondingly, vaginal tracts are relatively simple and straight. On the other hand, mallards Anas platyrhynchos frequently force ovary-bearing mallards into copulation. Their vaginas are full of blind pouches and are quite convoluted. Studies have shown that successful fertilization is drastically lower in waterfowl subjected to forced copulation by nonmates, and the explosive penile eversion we saw earlier in the chapter is actually stopped by those vaginal twists and turns.

Squamates, turtles, and crocodylians have paired ovaries and oviducts. However, squamates also often show some asymmetry. In lizards, it’s just slight, but in many snakes, the right oviduct is much longer than the left (Figure 17.42). In some squamates, the left oviduct is either vestigial or lost completely.

On the other hand, many extant birds only develop a functional left ovary and oviduct (Figure 17.40). The right oviduct and ovary develop early in development but quickly regress thanks to the secretion of AMH by the ovaries, which triggers apoptosis (cell death). The left ovary produces enough estrogen to protect itself from the effects of AMH. Again, this has been hypothesized to have something to do with making the body lighter for flight. However, we have to be careful not to generalize this to all birds! We know the most about birds that have been domesticated—chickens, geese, and ducks. The brown kiwi, some sparrows, the occasional pigeon, and some falcons retain both the right and left ovaries, although they are often asymmetrical. Note that all these birds except the kiwi are excellent fliers.

The oviducts, regardless of whether there are one or two, each open into the cloaca. This is also where we find the clitoris (or hemiclitoris, in the case of our squamates). Crocodilian clitorises lie ventrally in the cloaca and have the same general parts as crocodilian penises: paired crurae, a shaft, and a glans. Lizards have evertable hemiclitorises, much like lizard hemipenes. Like hemipenes, they lie caudal of the cloaca and have a sulcus and similar eversion/retraction mechanisms. Unlike some lizard hemipenes, there is no cartilaginous “bone.” Snake hemiclitorises are understudied at best, and until recently scientists weren’t sure whether they had one or not. We do know that they cannot be everted but do have erectile tissue that can be filled with blood.

We previously mentioned that all extant birds are oviparous, as are the other extant archosaurs (crocodylians). Does this mean that we should expect the nonavian dinosaurs to be oviparous as well? Probably! We know that there are fantastic fossils of dinosaur eggs, some including embryos in the eggs of theropods (carnivores), sauropods (long-necked), and hadrosaurs (“duck-billed”). What about the reproductive tracts? Birds and crocodylians have very different ones. Soft tissues rarely fossilize, so there are very few fossilized ovaries and oviducts in any bird, nonavian dinosaur, or reptile. However, evidence from fossilized nesting behavior and egg arrangement within dinosaur nests give us some clues. Unless the dinosaurs are moving their eggs within the nest in particular patterns, the pattern that eggs are arranged in the nest should reflect where they were oviposited. Some patterns are more likely to occur with two functional oviducts and others with one. Coupled with eggshell structure and particular types of egg pathologies, and comparing those to our extant archosaurs, it seems that sauropods may have had two functional oviducts, while theropods that are more closely related to birds likely only had one.

Mammals

As we should expect by now, much of the reproductive tract in ovary-bearing mammals is the same as other amniotes. Ovaries come in many shapes and sizes, and they vary with life stage. For example, an adult blue whale’s ovary weighs 30 kg while pregnant but a mere 7 kg when not pregnant. Mammals tend to have paired ovaries, although in the platypus (a monotreme), only the left is functional (Figure 17.43). Meanwhile, the other extant monotremes, the echidnas, have two functional ovaries.

Mammalian oviducts are generally divided into four regions (but hold that thought until you get to the next paragraph). Ova enter the oviduct at the infundibulum, then travel to the ampulla, isthmus, and utero-tubal junction (the border between the uterus and oviduct). The ampulla and isthmus are not always differentiated, and in humans, fertilization tends to happen in the ampulla. The oviduct is usually folded into rugae, especially near the utero-tubal junction; those rugae sometimes are used for sperm storage. Oviducts also come in many different shapes, including looped (bears and squirrels), coiled (pigs), bent (kangaroo rats, mink, pocket gophers), and straight (rabbits and humans).

Note that the uterus was left out of the oviduct divisions described above. The uterus is, as we’ve seen in other vertebrates, the fifth division of the oviduct. Yet it’s often treated as a separate organ completely. The rationale here is not clear—perhaps this is a holdover from naming organs and parts in humans without understanding the evolutionary history. Or perhaps this is because the uterus is where embryos develop in therian mammals, so it warrants its own consideration. Regardless, at this point in the chapter, you know that the uterus is indeed homologous to the uteri we’ve seen before, and as such it is part of the oviduct.

The uterus is more than a site of embryonic development in therians. It’s an organ that is active in just about everything happening with that embryo, from communication with other organs, to placenta formation (which we’ll get to later), to expelling both the fetus and placenta, and even maintaining microbial health. Like the other parts of the oviduct, there’s a lot of variation in uterine shape (Figure 17.44). Some mammals, such as primates and nine-banded armadillos, have a simplex uterus, where the halves are totally fused and there is only one cervix, the muscular boundary between the uterus and vagina. Other mammals have a duplex uterus, where the right and left uteri are totally separate, and each has their own cervix. This includes rabbits, rats, monotremes, and metatherians. We also see something in between, a bicornate (biconvex) uterus, where the right and left halves are partially fused. Where that fusion happens varies. Most commonly it’s the internal lumen, and we see that in ungulates of all sorts, cetaceans, and carnivorans. But wildebeest have separate lumens, two separate cervical canals, and then just one cervix. And narwhals and xenarthrans have no cervix at all.

After we leave the cervix and start heading out of the reproductive tract, there is usually a vagina that contains the same layers as the uterus except for an endometrium. However, monotremes do not have a vagina, and there is considerable variation in terms of what embryonic tissues contribute to which portions of the vaginal canal across mammals. Vaginas come in a lot of lengths, shapes, and sizes, although not as extreme as some of the birds we previously learned about. Metatherians have two separate vaginas to go with their duplex uteri with separate cervixes, with the exception of opossums that have two cervixes with three vaginas.

What happens next depends on which mammal you’re looking at. Some mammals—including the monotremes, tenrecs, porcupines, and pikas—retain a cloaca. Other mammals keep only a portion of the cloaca, called the urogenital sinus, a common opening for urinary and reproductive tracts. This opening is separated from the anus by a urorectal septum. This is seen in a wide range of mammals, including hippos, xenarthrans (anteaters, sloths, armadillos), rabbits, marsupials, and elephants. Still other mammals, including the primates, have three completely separate openings—the anus, the urethral meatus, and the vaginal vestibule (vestibulum).

Most mammals also have a clitoris, and we see just as much variation here as we have seen in mammalian penises (Figure 17.39). Most mammal clitoral erectile tissues are composed of paired corpora cavernosa and a corpus clitoridis that lies ventral to the urethra. Some mammals also have paired or fused crurae, which are structures that provide attachment to muscles that run to the pelvis. Much of the clitoral structure is internal and not externally visible (although see Box 17.3), but that does not mean it is a small organ. For example, elephants can have a clitoris up to 37 cm long! The external portion of the corpus clitoridis (also called the glans clitoris) varies in position. Sometimes it is in or on the rim of the vestibulum; other times it may be in the lumen of the urogenital sinus. Some mammals also have a bone or cartilage called the baubellum (or os clitoridis), similar to the baculum.

Box 17.3—Blurred Lines: Spotted Hyenas and Talpid Moles

At the beginning of this chapter, we discussed how sex is often assigned based on chromosomes or, in the case of humans, at birth based on the morphology of the external genitalia. You also just read about the general anatomy of ovary-bearing mammals. Just as we saw in other vertebrate groups, there is a lot of variation in anatomy across species (and within species!), and mammals are no exception. There are several mammal species where the ovary-bearing sex has external genitalia that more closely resemble that of the testes-bearing sex. This is often an enlarged clitoris, as we see in spider monkeys, bonobos, elephants, and various viverrids (civets, genets). Both spotted hyenas Crocuta crocuta and talpid (true) moles have both penis-like external genitalia and territorial, aggressive behavior. As such, they’ve been very well studied.

Moles have an elongated clitoris that encloses the urethra, and a prepuce that covers the urethral opening (Figure 17.45). The vaginal opening is separate and stays firmly shut unless it is breeding season. Interestingly, the moles have ovotestes instead of ovaries! These gonads are composed of both testicular (medullary) and ovary (cortical) tissue. The testicular tissue cannot make sperm, but it does make testosterone and has an underdeveloped epididymis. The rest of the reproductive tract is typical of ovary-bearing mammals, complete with oviducts, a bicornate uterus, and a uterovaginal canal.

Ovary-bearing spotted hyenas have an entirely different setup (Figures 17.46 and 17.47). Unlike moles, their clitoris (often referred to as a pseudopenis) can actually be erected. Hyenas also have a pseudoscrotum formed by the fusion of the urogenital folds—in many other mammals, these form the labia. In what may seem like a throwback to other vertebrates, hyenas have a urogenital sinus that opens at the tip of the clitoris. There is no separate vaginal opening. That means copulation, urination, and birth all happen through the same opening. The internal reproductive organs are fairly typical of mammals: two ovaries, two oviducts, a bicornate uterus, and a vaginal canal. However, the vaginal canal makes a hairpin, 180-degree turn such that successful birth of pups is very difficult.

As biologists have studied these two mammals, the inevitable question is, Why did this evolve? We tend to be skewed toward assuming that everything is an adaptation—a feature that was favored by natural selection for its current function. However, there are other possible explanations. Perhaps this is an exaptation, which is a feature that evolved for a particular use but is now used for something else. Or this could be a nonadaptation, in which the feature was not favored by natural selection at all. Stephen Jay Gould considered these concepts in his 1979 paper “The Spandrels of San Marco and the Panglossian Paradigm: A Critique of the Adaptationist Programme.”

For either our moles or spotted hyenas, pose a hypothesis that explains why these particular reproductive features evolved for each of our three concepts (adaptation, exaptation, and nonadaptation). How would you test each of your three hypotheses?

As you’ve now read earlier in this book, we divide our mammals up based on reproductive strategy. Monotremes, whose extant forms only include a few species of echidna and the platypus Ornithorhynchus anatinus, are oviparous. Theria includes the eutherians (placentals) and metatherians (marsupials), and both groups are viviparous. The term placentals for the Eutheria incorrectly implies that other mammals do not have placentas. In fact, while monotremes do not, marsupials do!

Placentas are pretty interesting organs. In mammals, they have a variety of functions, including nutrient transfer, immune system transfer, in utero communication, waste exchange, and gas exchange. As we saw in our viviparous squamates, both the embryo and the parent gestating said embryo contribute to the development of this organ. However, mammalian and squamate placentas are not homologous—the mammalian placenta arose independently from squamates, as squamates are diapsids and mammals are derived from synapsid reptiles. In mammalian placentas, the gestating parent’s endometrium contributes to the structure of the placenta, and for the embryo, all four extraembryonic membranes are involved. The chorion fuses with either the yolk sac (choriovitelline placenta, as “vitelline” means “yolk sac”) or the allantois (chorioallantoic placenta). In both eutherians and metatherians, the choriovitelline placenta is what is initially formed, and it persists to be the functional, final placenta in metatherians. In eutherians, the final placenta ends up as chorioallantoic (Figure 17.48). How much these extraembryonic membranes integrate with the parental endometrium is variable, ranging from just a little to enough integration that the parent’s blood vessels are eroded enough that parental blood ends up accumulating within the chorioallantois.

Marsupials are also known to have a short intrauterine gestation period (2–5 weeks), followed by young making their way to the marsupium (pouch) when present. It has been hypothesized that perhaps the choriovitelline placenta is less efficient than the chorioallantoic placenta, necessitating a quick exit from the uterus. However, that does not seem to be the case. First, there are rodents that have 3- to 4-week gestation periods. Second, if we focus on the neonates (recently born), we see wonderful adaptations associated with lactation (milk production), including highly developed olfaction and very functional forelimbs. Both of these allow the neonates to make their way from the vestibulum up to the mammary glands without parental help. It’s also worth remembering that the most recent common ancestor of metatherians and eutherians was sometime in the Jurassic or Early Cretaceous period. Our extant marsupials are pretty darn derived and shouldn’t be considered “primitive” to eutherians.

Speaking of lactation, this is something shared across mammalian species and is considered a synapomorphy. Mammary glands are composed of milk-secreting cells that line spaces called alveoli (not to be confused with those alveoli in your lungs). Alveoli are grouped together into lobules, and muscle fibers squeeze the alveoli to send milk to collecting ducts (Figure 17.49). These ducts send milk to pores (in monotremes), to nipples, or to storage organs called teats (think of cows and their udders). The number and placement of mammary glands vary across mammals, but they tend to occur in pairs. Unfortunately, mammary glands are soft tissues that do not fossilize particularly well. Thus, paleontologists use associated skeletal elements to indicate when this feature may have evolved. Specifically, we can look at the evolution of the secondary hard palate, which is associated with creating suction, and the development of deciduous (primary, baby) teeth. We see these for the first time in the Late Triassic and Early Jurassic stem mammal Morganucodon.

Let’s return to this idea of metatherians as lactation specialists. Extant marsupials make two types of milk. The first is called teat attachment milk, which is for when the neonates are attached to the teat 24 hours per day, starting when they first emerge from the vagina. The second type of milk is called intermittent sucking milk, for when the neonates are not constantly attached to the teat and may even leave the marsupium. Kangaroos can make both kinds of milk at the same time but at different teats. This isn’t something that eutherians can do.

17.5 Humans

Truthfully, human reproductive systems are not very different from those of other eutherians. As with many other systems, some components have special names because the Western scientists who named them did not understand their homology to other organisms’ anatomy (such as Fallopian tubes, which are just oviducts). Thus, ovaries shed their eggs into the coelom, where the fingerlike fimbrae of the oviduct are ready to sweep the egg into the tube. Like sloths, some bats, and our fellow primates, humans have a simplex uterus with a cervix at the boundary between the uterus and vagina (Figure 17.50). The cervix is composed of a ring of cartilage encased in tissue. Humans have a straight, rugose vagina composed of connective tissue, muscle, nerves, and blood vessels. Several glands, such as the Bartholin’s glands and lesser vestibular glands, secrete mucus that serves to keep the vagina moist to support the extensive microbiota and to protect the vagina from trauma.

Collectively, the external genitalia of ovary-bearing mammals are called the vulva (Figure 17.51). In humans, the external opening to the vagina is enclosed in folds of skin called the labia (singular: labium); there are two sets of folds, the labia majora and labia minorum. The labia also enclose the visible portion of the clitoris. Also included in the external genitalia category are the mons pubis, a pad of fatty tissue that sits over the pubis, and a hymen, which is a thin membrane that may partially cover the vaginal entrance. Ovary-bearing humans also have a pair of greater vestibular glands (also known as Bartholin’s glands), which are homologous to bulbourethral glands in testes-bearing humans; these glands are located lateral to the vaginal opening and similarly produce a mucous-like secretion that acts as a lubricant. The lesser vestibular glands (also known as Skene’s glands) are homologous to the prostate gland found in testes-bearing mammals. The function of these glands is less clear; it is hypothesized that they also produce ejaculate and act as an antimicrobial. We did not mention these glands previously, as they are very poorly studied in any mammalian taxa.

Many ovary-bearing humans menstruate (eumenorrhea) during a portion of their lifetimes, shedding the endometrium and growing a new one in 21- to 50-day cycles—the 28-day cycle is a statistical average, but few people actually have a cycle of this exact length, and it can vary within one’s lifetime. The shed endometrium passes through the cervix and vagina and then out. Again, humans are not unique here, as eumenorrhea occurs in primates, hedgehogs, carnivorans, quolls, and some groups of bats.

For sperm-producing humans, per usual, we start with the testes, which are encased in an external scrotum (Figure 17.52). Sperm move from the seminiferous tubules to the rete testes, a network of tubules, and then the efferent ductules, and then to the epididymis. Sperm are stored in the epididymis until ejaculation, when smooth muscle contractions push the sperm into the vas deferens.

Remember what we learned from the descent of the testes—that those testes were pulled through the inguinal canal in the abdominal wall. Thus, the vas deferens passes through the inguinal canal and heads to the pelvic cavity, where each vas ends in an ampulla, a small bladder-like sac (Figure 17.53). Seminal vesicles secrete fructose-rich fluid into the ampullae. The ducts of the seminal vesicles and ampullae combine to form a short ejaculatory duct, which then leads to the prostate gland. The prostate in humans is about the size of a walnut and secretes more fluid to the semen. Prior to ejaculation, a pair of bulbourethral glands (also known as Cowper’s glands) release preejaculate fluid that removes urine and lubricates the penis. Human penises are largely identical to other mammalian penises in terms of their structure and erectile tissue. Unlike many other mammals, humans do not have a baculum, spines, or other hard materials.

17.6 Integration

The gonads serve as endocrine organs as well and interplay with a whole host of things in your body. You can read more about this in Chapter 18. However, we want to draw your attention to another site of integration: mammalian pelvises. As you learned in Chapter 10, the evolution of the pelvic girdle had big implications for locomotion. However, once that pelvis is in place and the limbs articulate with it, various tubes and nerves have to pass through it to accomplish urination, defecation, and in ovary-bearing tetrapods, oviposition (egg-laying) or parturition (birth). This means that the pelvis itself is subject to numerous selective pressures.

Human parturition is complex in large part due to the shape of the pelvis. As the fetus passes from the uterus through the vagina to its hopeful exit, it undergoes a complex rotation. Assuming it is entering the vagina headfirst, the head rotates, then the shoulders, then the rest of the body. This is due to the changing shape of the pelvis as the fetus passes through the inlet, midplane, and outlet (also known together as the birth canal or pelvic canal)—the inlet’s longest axis is oriented mediolaterally, while the outlet’s longest axis is oriented anteroposteriorly (Figure 17.54). Meanwhile, the midplane is narrower than either the inlet or outlet. The shape changes are largely due to ischial spines, ischial tuberosities, and sacrum all being in the way. The fetus barely fits through these openings, and this can cause injury or death to the fetus or the birthing parent. However, if we look at the great apes, our closest relatives, the birth canals of their ovary-bearing individuals are roomier, and the long axis remains in the anteroposterior direction. This is true of other primates, including both New- and Old-World monkeys as well.

Unfortunately, a large birth canal, associated with larger pelvic floor muscles, is not ideal for bipedal locomotion. As we shift to a bipedal posture, more of our weight is stacked above the pelvis. The larger pelvic floor cannot handle the stress and strain associated with this shift in force distribution. In addition, some studies have shown that a shorter distance between hip joints is more energy-efficient for bipedal locomotion and that a shorter anteroposterior length in the inlet allows for less pelvic tilt and a more stable posture, as it better supports the vertebral column.

The shape of the pelvis also has implications for locomotion-related injuries in humans. Often we see differences in pelvis shape between ovary-bearing and testes-bearing humans—something called sexual dimorphism (= two shapes). Not only do the pelvises of human egg producers have a wider pelvic canal, but they also tend to have a sacrum that is shorter and oriented more posteriorly, a smaller acetabulum, a larger distance between acetabulae, and a larger subpubic angle (Figure 17.55).

That leads to sex differences in the muscles of the lower limbs. For example, recall from Chapter 12 that the quadriceps femoris (what you may know as your quads) originates on the ilium, just superior to the acetabulum. The heads of your quads insert on the patella via a common tendon. Given the difference in pelvic shape, we should expect differences in the “Q angle,” or the angle that the line of action of the quadriceps makes with the patellar tendon (Figure 17.56). Indeed, we see that ovary-bearing humans have a higher Q angle than testes-bearing humans by just a few degrees (a mean of 17 vs. 14 degrees, respectively, albeit with a lot of variation). However, those few degrees make a big difference, corresponding to an increased prevalence of anterior cruciate ligament (ACL) injuries in ovary-bearing humans, as it puts a bit more torque on the knee joint.

17.7 Summary

The vertebrate reproductive system is integrated with the urinary system, with some ducts being co-opted to carry gametes and the shift from a fully aquatic lifestyle to a terrestrial one. Even with those shifts as driving forces in the evolutionary trends we see, there is tremendous variation within vertebrate groups.

17.8 Further Reading

1. Clancy, Kate B. H. 2023. Period: The Real Story of Menstruation. Princeton: Princeton University Press, 2023.
2. Graves, J. A. Marshall, and S. Shetty. “Sex from W to Z: Evolution of vertebrate sex chromosomes and sex determining genes.” Journal of Experimental Zoology 290 (2001): 449–462.
3. Hayssen, Virginia D., and Teri J. Orr. Reproduction in Mammals: The Female Perspective. Baltimore: Johns Hopkins University Press, 2017.
4. Judson, Olivia. Dr. Tatiana’s Sex Advice to All Creation. New York: Macmillan, 2002.
5. Kanamori Akira l., and Yasuhisa Kobayashi. “Gamete-exporting organs of vertebrates: Dazed and confused.” Frontiers in Cell and Developmental Biology 11 (2023): 1328024.

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