Internal fertilization is a reproductive process in animals where the fusion of male sperm and female egg occurs within the body of the female parent, contrasting with external fertilization that takes place outside the body in an aqueous environment.[1] This mechanism typically involves the male depositing sperm directly into the female's reproductive tract via copulation, spermatophore transfer, or other specialized methods, ensuring gamete union in a protected internal setting.[2]Internal fertilization is most common in terrestrial animals, such as mammals, birds, reptiles, amphibians like salamanders, insects, and spiders, but it also occurs in certain aquatic species including sharks, rays, and cetaceans like whales and dolphins.[2] The process supports three primary developmental strategies: oviparity, in which fertilized eggs are laid and develop externally after deposition; viviparity, where embryos develop internally and offspring are born live, nourished by the mother; and ovoviviparity, where eggs develop and hatch inside the female without direct maternal nourishment of embryos.[1] These strategies allow for varying degrees of parental investment and protection, with viviparity often seen in mammals and some reptiles, while oviparity predominates in birds and many reptiles.[3]One key evolutionary advantage of internal fertilization is the protection of gametes and early embryos from dehydration and environmental predators, which was crucial during the transition from aquatic to terrestrial habitats.[4] This method enhances fertilization success rates by limiting sperm dispersal and enabling precise mate selection, though it generally results in fewer offspring compared to external fertilization due to higher energy costs for internal development and care.[3] In species with internal fertilization, females often exhibit greater control over reproduction, including the potential for sperm storage and selective fertilization, which influences mating behaviors and genetic diversity.[2]
Overview
Definition
Internal fertilization is a mode of sexual reproduction in which the union of male and female gametes—sperm and egg—occurs within the body of the female parent, typically in her reproductive tract.[5] This process generally involves the deposition of sperm directly into the female via copulation or insemination, allowing the sperm to encounter and fertilize the egg internally rather than in an external aqueous environment.[2] In most cases, this occurs in terrestrial or semi-terrestrial animals, though it is also present in some aquatic species.[6]A core characteristic of internal fertilization is the fusion of gametes in a protected internal environment, which shields the developing zygote from external threats such as desiccation or predation.[7] This often necessitates specialized reproductive structures to facilitate sperm transport, storage, and interaction with the egg; for example, in many invertebrates like insects, spermathecae serve as sperm-storage organs connected to the oviduct, while in vertebrates such as mammals, fertilization typically takes place in the oviduct (fallopian tube).[8] These adaptations ensure efficient gamete encounter and support subsequent embryonic development, either within the female's body or after egg-laying.[9]The concept of internal fertilization was first articulated in observations of viviparous (live-bearing) animals by ancient naturalists, notably Aristotle in the 4th century BCE, who described seminal contributions to reproduction in such species in his work On the Generation of Animals.[10]
Comparison with External Fertilization
External fertilization involves the release of sperm and eggs into an external medium, typically water, where the gametes fuse outside the parents' bodies in a process known as spawning. This mode is prevalent among aquatic species, including most fish and amphibians, where both sexes discharge gametes simultaneously into the surrounding water to facilitate encounter and fertilization.[2]A primary distinction lies in the environmental control and risk mitigation: internal fertilization occurs within the female's reproductive tract, offering a protected setting that minimizes exposure to desiccation, predation, and environmental stressors on the gametes. In contrast, external fertilization exposes gametes to dilution, currents, and predators, necessitating the production of vast quantities of gametes—often millions per individual—to compensate for low encounter probabilities and achieve viable fertilization rates.[4][2]Internal fertilization predominates in terrestrial and aerial habitats, enabling reproduction away from water bodies by preventing gamete drying, while external fertilization is confined largely to aquatic settings where water serves as a transport medium. For instance, sea urchins employ broadcast spawning, synchronously releasing millions of eggs and sperm into seawater to counter dispersion by waves and tides.[4][11]Fertilization success per gamete is generally much higher in internal modes, reaching 70–80% in mammals under controlled conditions representative of natural internal processes, compared to external broadcast spawners where rates can vary from 0% to 100% and often fall below 20% in low-density or adverse conditions due to gamete dilution.[12][13]
Evolutionary Aspects
Origins and Evolution
Internal fertilization first appeared in the fossil record during the early Cambrian period, approximately 521 million years ago, among early arthropods. Evidence from exceptionally preserved fossils, such as those from the Burgess Shale, reveals copulatory structures like clasper-like appendages in trilobites, suggesting that males used these to grasp females and facilitate sperm transfer, marking a transition from external fertilization in aquatic ancestors.[14][15] This early innovation likely arose in marine environments, where internal methods provided advantages in gamete protection amid increasing ecological complexity.[16]The transition to terrestrial habitats during the Devonian period, around 400 million years ago, represented a pivotal selective pressure on reproductive strategies, particularly for early tetrapods evolving from aquatic ancestors. Adaptations to prevent gamete desiccation were crucial, though internal fertilization in amphibians evolved variably across lineages, with some retaining external modes.[17]Phylogenetically, internal fertilization exhibits convergent evolution across diverse animal groups, including insects, reptiles, and mammals, driven by environmental challenges rather than shared ancestry. It is absent in most basal deuterostomes, such as cephalochordates, but occurs indirectly in some echinoderms through mechanisms like spermatophore transfer or brooding that internalize gamete fusion.[16]Fossil evidence of copulatory organs in Cambrian arthropods complements genetic data indicating multiple independent origins of internal fertilization. Molecular clock analyses estimate origins in pancrustaceans around 450 million years ago, aligning with arthropod diversification.[16]
Adaptive Significance
Internal fertilization provides a key adaptive advantage by protecting gametes and embryos from environmental hazards, particularly in terrestrial or variable aquatic environments. By enabling sperm to be deposited directly into the female reproductive tract, it shields gametes from desiccation, ultraviolet (UV) radiation, and pathogens that would otherwise compromise fertilization success in external settings. In amphibians, parental care behaviors, such as egg wrapping in newts (Triturus spp.), minimize UV-B penetration and enhance embryo survival, while internal processes in some species limit pathogen exposure.[18] Overall, these mechanisms facilitated the evolutionary shift to terrestrial reproduction across vertebrates, reducing reliance on stable aquatic habitats.[18]Another significant benefit is increased fertilization efficiency, which minimizes energy expenditure on gamete production and enhances reproductive success in resource-limited conditions. Internal fertilization permits precise sperm delivery to the site of egg fertilization, contrasting with the wasteful mass release required in external modes, where much sperm is lost to dilution or predation. In vertebrates, this precision correlates with evolved sperm traits, such as elongated heads (1.4 times longer) and midpieces (18 times longer), which improve motility and ATP production for navigation through viscous female tracts, allowing a single copulation to fertilize multiple eggs effectively.[19] For example, in internally fertilizing fish and tetrapods, sperm longevity extends from hours to days or years, optimizing energy use and reducing the need for frequent matings compared to broadcast spawners.[19]Internal fertilization also promotes mate choice and genetic quality assurance through pre- and post-copulatory selection mechanisms, driving sexual selection and evolutionary refinement of reproductive traits. It facilitates cryptic female choice, where females bias fertilization toward preferred males' sperm via tract physiology or seminal fluid interactions, intensifying sperm competition within the reproductive tract.[20] In vertebrates, this post-ejaculatory competition selects for superior sperm morphology and function, as seen in elongated sperm components that enhance competitive performance, ultimately improving offspring genetic quality.[19] Unlike external fertilization, where mate assessment is limited to visual or behavioral cues, internal modes allow females to exert control over paternity, reducing risks from low-quality mates and promoting adaptive genetic diversity.[20]Furthermore, internal fertilization correlates with the evolution of complex social behaviors, including pair bonding and biparental care, which amplify offspring survival in challenging habitats. In amphibians like poison frogs (Dendrobatidae, e.g., Ranitomeya imitator), external fertilization with biparental care, such as tadpole transport and feeding in phytotelmata, supports monogamous pair bonds where ecological constraints favor cooperative investment.[18] This linkage extends to birds, where internal fertilization underpins long-term pair bonding in many monogamous species, enabling shared incubation and provisioning that enhances fledging success rates compared to uniparental care. Such behaviors evolve because internal modes increase paternity certainty, incentivizing male investment and reducing extra-pair mating risks, thereby stabilizing social units for enhanced parental effort.[20]
Mechanisms
Methods of Internal Fertilization
Internal fertilization in animals is achieved through several distinct methods that facilitate the union of sperm and egg within the female's body, primarily to protect gametes from environmental hazards. One of the most widespread techniques is copulation, involving direct intromission of male reproductive structures into the female's genitalia. In many insects, this occurs via specialized intromittent organs that deposit sperm directly into the female reproductive tract during mating.[21] Similarly, in reptiles such as snakes, males utilize paired hemipenes—evertible structures housed in the tail base—that are inserted into the female cloaca to transfer sperm, enabling precise insemination and often alternating between the two hemipenes during a single copulatory event.[22] This method predominates in terrestrial arthropods and squamate reptiles, where physical coupling ensures efficient sperm delivery and minimizes loss.[2]Another key approach is indirect insemination via spermatophores, which are encapsulated sperm packets produced by the male and subsequently internalized by the female. In scorpions, males deposit these gelatinous spermatophores on the substrate during a courtship dance, after which the female positions her genitalia to uptake the packet, allowing sperm to migrate internally for fertilization.[23] Salamanders (order Urodela) employ a similar strategy, where the male places a stalked spermatophore on the ground or in water, and the female retrieves it using her cloaca, facilitating internal fertilization without direct genital contact. This indirect method reduces physical risks associated with direct copulation and is adaptive in species with limited mobility or aquatic-terrestrial transitions, though it requires precise behavioral synchronization to succeed.[23]A more specialized and costly variant is traumatic insemination, where males bypass conventional genitalia by injecting sperm directly through the female's body wall. In bed bugs (Cimex lectularius), males use a needle-like paramere to pierce the female's abdomen, depositing sperm into a specialized ectodermal invagination called the spermalege, which channels it to the ovaries.[24] This hypodermic method, while ensuring fertilization, inflicts wounds that increase female mortality and immune stress, leading to evolutionary counter-adaptations like the spermalege to mitigate injury.[24] Traumatic insemination highlights sexual conflict, as males gain reproductive advantages at the expense of female fitness, and is rare but convergent across taxa like certain heteropteran insects.[25]
Sperm Transfer and Insemination
Sperm transfer in internal fertilization involves specialized anatomical structures in males that deliver sperm directly into the female reproductive tract, ensuring proximity to the eggs and protection from environmental hazards. In vertebrates such as mammals, the penis serves as the primary intromittent organ, facilitating the deposition of semen into the female vagina during copulation.[8] Similarly, in elasmobranch fishes like sharks and rays, paired claspers—elongated modifications of the pelvic fins—function as intromittent organs, with one clasper typically inserted into the female's cloaca to transfer sperm via a grooved channel.[26] In livebearing teleost fishes, such as guppies (Poecilia reticulata), the gonopodium, a modified anal fin, acts as a copulatory organ that inserts into the female gonopore to eject sperm packets directly into her ovarian cavity.[27]In invertebrates, male structures vary widely; for instance, many insects employ an aedeagus, a sclerotized intromittent organ that penetrates the female genital opening to deposit sperm, often in conjunction with spermatophores for indirect transfer.[28] Female receptacles for sperm reception are equally diverse, typically involving the oviducts or specialized bursae. In mammals and birds, sperm are received in the upper oviducts or uterine regions, where they await ovulation.[8] Among crustaceans, such as the Dungeness crab (Metacarcinus magister), paired bursae adjacent to the oviducts serve as initial reception sites for spermatophores, distinct from deeper storage structures.[29]Behavioral sequences preceding sperm transfer often include courtship rituals that align the partners for mounting or packet uptake, enhancing successful insemination. In poeciliid fishes, males perform sigmoid displays and nips to orient the female, leading to gonopodium insertion that lasts mere seconds.[30] Insect mating, as in fruit flies (Drosophila melanogaster), involves rapid courtship dances followed by copulation durations of approximately 20 minutes, during which sperm transfer occurs primarily in the first 5 minutes.[31] Mammalian copulation exhibits greater variability, ranging from brief insertions in rodents (under 1 minute) to prolonged intromissions in larger species like lions, lasting up to several hours, influenced by body size and social context.[32]Adaptations for multiple inseminations are common in polyandrous species, where mechanisms like sperm displacement allow subsequent males to remove or displace prior ejaculates. In Drosophila melanogaster, the male's aedeagus features spines that physically displace rival sperm from the female's reproductive tract during remating, conferring a competitive advantage to the last male.[33] Such strategies evolve under postcopulatory sexual selection, optimizing paternity in systems where females mate with multiple partners.[34]
Unique Physiological Processes
Internal fertilization involves several specialized physiological processes that ensure successful gamete interaction and prevent pathological outcomes, distinct from those in external fertilization systems. These processes include modifications to sperm for fertilization competence, mechanisms to limit multiple sperm entries, prolonged sperm viability in the female tract, and the initiation of embryonic development upon gamete fusion.Sperm capacitation refers to the series of biochemical and physiological changes that mammalian sperm undergo in the female reproductive tract to gain fertilizing ability. This process is essential for enabling hyperactivated motility and the acrosome reaction, which allows sperm to penetrate the egg's protective layers. A key event in capacitation is the efflux of cholesterol from the sperm plasma membrane, facilitated by proteins in the uterine and oviductal fluids, such as albumin and lipoproteins, which reduce the cholesterol-to-phospholipid ratio and increase membrane fluidity.[35] This cholesterol removal is critical, as freshly ejaculated sperm retain a stabilizing cholesterol layer that must be stripped for capacitation to proceed, typically taking hours in the female tract.[36] Additional changes include protein tyrosine phosphorylation and ion influxes, such as calcium and bicarbonate, which collectively prepare the sperm for egg binding without external environmental triggers.[37]To prevent polyspermy—the entry of multiple sperm into a single egg, which would lead to lethal chromosomal imbalances—internal fertilization employs dual blocking mechanisms: a rapid "fast block" and a slower, more permanent "slow block." The fast block occurs immediately upon sperm-egg fusion through depolarization of the egg's plasma membrane, creating an electrical barrier that repels additional sperm for several minutes.[38] In mammals, this is complemented by the slow block, initiated by the release of cortical granules from the egg periphery, which modify the zona pellucida—an extracellular matrix surrounding the egg—via enzymatic actions like proteolysis of glycoproteins ZP2 and ZP3.[39] This zona reaction hardens the matrix and removes sperm-binding sites, ensuring only one sperm fertilizes the egg and maintaining genomic integrity.[40]Sperm storage allows females to maintain viable sperm for extended periods post-insemination, a adaptation prominent in reptiles where spermathecae—specialized oviductal tubules—can sustain sperm for months to years. In species like turtles and squamates, these structures provide a nutrient-rich environment through glandular secretions containing sugars and proteins that support sperm metabolism and motility.[41] Mechanisms for long-term viability also involve immune modulation, such as localized suppression of inflammatory responses to prevent phagocytosis of sperm as foreign bodies, achieved via anti-inflammatory factors in the spermathecal fluid.[42] For instance, in the yellow-spotted river turtle, sperm stored for up to four years remain fertile, enabling asynchronous reproduction without repeated matings.[43]Egg activation in internal fertilization is triggered solely by intracellular signals from sperm-egg fusion, bypassing external stimuli required in some broadcast systems. Upon fusion, sperm introduce factors like phospholipase C zeta (PLCζ), which hydrolyze PIP2 to generate IP3, releasing calcium from the egg's endoplasmic reticulum and inducing oscillatory calcium waves.[44] These Ca²⁺ oscillations, lasting minutes to hours, activate key developmental processes including the completion of meiosis, cortical granule exocytosis for polyspermy block, and zygotic genome transcription, all without reliance on osmotic or chemical external cues.[45] In mammals, this precise signaling ensures robust embryo initiation in the controlled internal environment.[46]
Reproduction Outcomes
Expulsion Mechanisms
In internal fertilization, expulsion mechanisms refer to the processes by which fertilized eggs, embryos, or developed young are released from the female reproductive tract after internal development. These mechanisms vary across taxa and reproductive modes, ensuring the survival of offspring by balancing protection, nourishment, and timely release. The primary modes include oviparity, ovoviviparity, and viviparity, each adapted to different environmental and physiological demands.[47][48]Oviparity involves the laying of fertilized eggs outside the body following internal fertilization, where the eggs are encased in protective shells or membranes and develop externally using yolk reserves. In reptiles, for example, the amniotic egg features extraembryonic membranes such as the amnion, chorion, and allantois, which provide structural support, prevent desiccation, and facilitate gas exchange, while the leathery or calcified shell offers mechanical protection against predators and environmental hazards. This mode allows females to deposit multiple eggs in suitable locations, reducing prolonged maternal investment during development.[47][49]Ovoviviparity entails the internal retention and development of eggs within the female until hatching, after which live young are expelled without significant maternal nutrient provisioning beyond the initial yolk. In many sharks, such as those in the order Lamniformes, embryos develop inside eggshells within the uterus, nourished initially by the yolk sac and often supplemented by oophagy (consumption of unfertilized eggs), which supplies lipids and proteins until the young hatch and are born as miniature adults. This strategy enhances offspring protection from external threats during early stages while avoiding the metabolic costs of placental nourishment.[50][51]Viviparity features the live birth of fully developed young, with embryos nourished internally through maternal structures like placentas or extended yolk sacs, with cleavage patterns varying by taxon (holoblastic in mammals with minimal yolk, meroblastic in reptiles and fish with larger yolk reserves). In eutherian mammals, a chorioallantoic placenta facilitates nutrient and gas exchange between maternal and fetal blood supplies, supporting extended gestation until the young are sufficiently mature for expulsion. Mechanisms such as these enable higher offspring viability in variable environments but demand substantial maternal energy.[52][53]The timing and triggers of expulsion are regulated by hormonal signals that coordinate uterine or oviductal contractions. In mammals, declining progesterone levels remove inhibition on smooth muscle, while oxytocin release from the posterior pituitary stimulates powerful myometrial contractions during parturition, propelling the young outward. Variability in retention duration spans from mere hours post-fertilization in oviparous insects, where eggs are expelled shortly after internal insemination for external development, to over 22 months in elephants, reflecting adaptations to life history strategies like rapid reproduction versus prolonged nurturing.[48][54][55][56]
Development and Parental Investment
In species employing internal fertilization, embryonic development can follow either direct or indirect modes. Direct development results in offspring hatching or being born as miniature versions of adults, bypassing a free-living larval stage, which is common in many reptiles and viviparous fish where internal retention provides a protected environment for organogenesis.[2] This protection shields the embryo from environmental stressors, enabling the formation of complex structures like the amniotic sac in amniotes. In contrast, indirect development involves a larval stage post-hatching or birth, as seen in some internally fertilizing amphibians and invertebrates, where the larva undergoes metamorphosis; however, internal fertilization facilitates more intricate organ development compared to external modes by minimizing exposure to predators and desiccation.[57]Nutrient provisioning during development varies between lecithotrophy and matrotrophy. Lecithotrophy relies on yolk reserves supplied maternally prior to fertilization, supporting autonomous embryonic growth, as in oviparous reptiles like many snakes where eggs are laid with sufficient yolk for direct development.[58] Matrotrophy, conversely, involves post-fertilization transfer of nutrients from maternal tissues, often via placental structures, enhancing offspring size and survival; a prominent example is the evolution of the chorioallantoic placenta in eutherian mammals around 160 million years ago, enabling prolonged gestation and sophisticated fetal-maternal exchange.[59][60] In viviparous teleost fishes such as goodeids, matrotrophy can increase embryonic dry mass by over 1,000-fold through structures like the trophotaenium.[61]Parental investment post-fertilization spans a wide spectrum, from minimal to intensive care. Many internally fertilizing species exhibit no further parental care, such as reptiles that abandon eggs after oviposition, relying on the protective eggshell for incubation.[62] At the other extreme, extensive brooding occurs, exemplified by male pregnancy in seahorses (Syngnathidae), where males nourish and protect embryos in a specialized brood pouch, investing more energy than females and improving offspring viability through osmoregulation and gas exchange.[63] This male-biased care represents patrotrophy, a form of paternal nutrient provisioning rare but significant in syngnathids.[61]The energetic demands of internal development typically lead to higher parental investment, resulting in fewer but higher-quality offspring compared to external fertilization strategies. Parents allocate substantial resources to protection and nourishment, incurring costs like reduced mobility and increased predation risk, which correlate with smaller clutch sizes but enhanced juvenile survival rates.[2] In mammals and viviparous fish, this investment supports advanced organogenesis and larger neonates, trading quantity for individual fitness gains.[64]
Advantages and Disadvantages
Benefits
Internal fertilization offers higher fertilization success rates compared to external fertilization, often approaching near-complete efficiency in many species while conserving gametes by requiring fewer to achieve reproduction. This efficiency arises because sperm are delivered directly to the eggs within the female's reproductive tract, minimizing losses to environmental factors or dilution in water. In contrast, external fertilization in aquatic environments frequently results in low success, with many gametes failing to meet due to currents, predation, or timing mismatches.The internal environment provides substantial protection for the zygote against predators and abiotic stresses, such as desiccation or temperature fluctuations, thereby enhancing overall viability and survival. For instance, in oviparous frogs like Eleutherodactylus coqui, internal fertilization enables direct development on land, bypassing vulnerable aquatic larval stages and reducing predation risk on embryos and juveniles. This buffered development can dramatically improve offspring survival in terrestrial or variable habitats.[65]Genetically, internal fertilization facilitates mate guarding, where males can ensure paternity by remaining with the female during her receptive period, thereby reducing sperm competition from rivals and boosting individual reproductive success. It also supports sexual selection by allowing complex courtship displays and ornaments that signal male quality, as females can more selectively choose partners before insemination. Additionally, by limiting gamete dispersal, internal fertilization lowers the risk of hybridization with non-conspecifics, preserving genetic integrity and species-specific adaptations.[66]From a demographic perspective, internal fertilization aligns with K-selection strategies, enabling species to produce smaller clutch sizes but invest more resources per offspring for improved quality and survival in stable or resource-limited environments. This shift prioritizes fewer, higher-quality progeny over mass production, enhancing long-term population fitness in habitats where parental care or protection can be extended.
Drawbacks
Internal fertilization, while offering certain protective advantages, carries significant risks of disease transmission due to the intimate physical contact required between mating partners. Sexually transmitted diseases (STDs) can spread more readily through direct exchange of bodily fluids during copulation, potentially leading to severe health consequences for both sexes. For instance, in koalas, Chlamydia pecorum and Chlamydia pneumoniae are primarily transmitted sexually, causing reproductive tract infections, infertility, and even population declines in affected wild groups.[67] These examples illustrate how the close proximity and fluid exchange inherent to internal fertilization facilitate pathogen transfer, contrasting with the more diffuse risks in external fertilization modes.[68]The process also imposes substantial energetic costs on individuals, particularly females, as copulation, gestation, and associated parental care demand high resource allocation that can limit reproductive frequency. In mammals, gestation alone can require up to 90% of a female's metabolic budget in indirect costs, including maintenance of pregnancy and recovery, far exceeding the demands of external fertilization where gametes are simply released.[69] This elevated energy expenditure often results in extended intervals between breeding cycles; for example, large mammals like African elephants (Loxodonta africana) typically reproduce only every 3–5 years due to the prolonged 22-month gestation and lactation periods that deplete fat reserves and necessitate extensive foraging recovery.[70] Such constraints reduce overall lifetime fecundity compared to species employing external fertilization, where multiple spawning events can occur annually with lower per-event investment.[71]Behaviorally, internal fertilization creates dependencies that can hinder mating opportunities and introduce social tensions. The necessity to locate and attract a compatible mate in often low-density populations increases search costs and vulnerability to predation during courtship displays or travel. In sparse habitats, this mate-location challenge can drastically lower encounter rates. Furthermore, the physical act of copulation enables sexual coercion, where males use force, harassment, or intimidation to gain mating access, often at the expense of female autonomy and safety. This tactic is prevalent across internally fertilizing taxa, including primates and ungulates, leading to injuries, stress, and suboptimal mate choice that compromises genetic fitness.[72] Such dynamics highlight the interpersonal costs embedded in the reproductive strategy.Pathological risks arise from the internal navigation of gametes and embryos, which can result in anatomical complications unique to this mode. Ectopic pregnancies, where the fertilized egg implants outside the uterus—most commonly in the fallopian tubes—occur in mammals due to disruptions in oviduct transport following internal insemination, potentially causing tubal rupture and life-threatening hemorrhage if untreated.[73] Risk factors include prior infections or structural anomalies that block or narrow the reproductive ducts, increasing ectopic incidence by up to 10-fold in cases of unilateral tubal occlusion.[74] Additionally, blocked ducts, such as in the oviducts or epididymis, can lead to gamete retention, inflammation, or infertility; for example, salpingitis from ascending infections post-mating obstructs sperm or egg passage, further elevating reproductive failure rates in affected individuals.[75] These internal vulnerabilities underscore the trade-offs of enclosing fertilization within the body, where precision in physiological processes is paramount to avoid such outcomes.
Occurrence in Animals
Invertebrates
Internal fertilization is prevalent among many invertebrate phyla, enabling adaptations to diverse environments, particularly terrestrial and aerial habitats. In arthropods, which represent the largest group exhibiting this mode, sperm transfer often occurs via spermatophores—gelatinous packets containing sperm that males deposit during mating. For instance, in lepidopteran insects such as butterflies, males produce spermatophores in accessory glands to deliver sperm and seminal fluids, enhancing reproductive success by protecting gametes and influencing female physiology.[76] In contrast, spiders typically employ direct insemination, where males use modified pedipalps to insert sperm into the female's reproductive tract, fertilizing eggs as they pass through the oviduct.[77] Some arthropods, including certain insects like crickets and spiders, incorporate nuptial gifts—nutritive offerings such as prey or glandular secretions—during copulation to prolong mating and increase sperm transfer efficiency.[78]Among mollusks, internal fertilization is characteristic of cephalopods, where males utilize a specialized arm called the hectocotylus to transfer spermatophores directly into the female's mantle cavity.[79] In octopuses, this process allows precise sperm placement near the oviducts, facilitating fertilization of eggs that are subsequently brooded.[80] However, most bivalves rely on external fertilization, releasing gametes into the water column, though some brooding species may achieve internal fertilization by drawing in sperm.[81]In annelids, particularly clitellates like earthworms, internal fertilization occurs through mutual sperm exchange during copulation, followed by the clitellum secreting a mucus ring that forms a cocoon for egg deposition and fertilization.[82] This mechanism protects developing embryos in terrestrial or moist environments. Echinoderms exhibit external fertilization; most asteroids (sea stars) broadcast gametes externally, but in some brooding species, males release sperm near the female's brooded eggs to facilitate localized external fertilization, though this is exceptional and not widespread.Overall, internal fertilization dominates in invertebrates, with over 80% of insect species—arthropods comprising the majority of animal diversity—employing it to support aerial and terrestrial reproduction by storing sperm in female spermathecae for delayed egg fertilization.[55]
Fish
Internal fertilization is relatively uncommon among fish species, occurring in approximately 500 of the over 33,000 bony fish (Osteichthyes) species, and in all approximately 1,200 chondrichthyan species, including sharks, rays, and chimaeras.[83][84] This mode of reproduction is particularly prevalent in the family Poeciliidae among bony fishes, which includes around 300 livebearing species, and across all Chondrichthyes, where it is the universal reproductive strategy.[85] In contrast, the vast majority of fish species rely on external fertilization, releasing gametes into the aquatic environment.[83]Key adaptations facilitate internal fertilization in these groups. In poeciliid fishes, such as guppies (Poecilia reticulata), males possess a gonopodium—a specialized, elongated anal fin modified into an intromittent organ—that enables precise sperm transfer during insemination.[86] This structure allows for copulation-like mating, enhancing fertilization efficiency in freshwater and brackish environments. In chondrichthyan fishes, particularly sharks, males use paired claspers, extensions of the pelvic fins, to deliver sperm internally; these organs insert into the female's cloaca during mating.[87] Some carcharhinid sharks exhibit aplacental viviparity, where embryos develop without a direct placental connection to the mother, relying instead on yolk reserves and limited histotroph.[88]The reproductive processes in internally fertilizing fish often involve extended internal gestation and specialized nutrient provisioning. Gestation periods can reach up to two years in certain shark species, such as the gulper shark (Centrophorus granulosus), allowing for advanced embryonic development within the female's uterus.[89] In viviparous species, including some sharks like the white shark (Carcharhinus carcharias), embryos receive supplemental nutrition through uterine milk—a lipid-rich secretion from the maternal uterine lining—supporting growth beyond initial yolk supplies.[90] A notable example is the guppy (Poecilia reticulata), which demonstrates superfetation, enabling females to carry multiple broods at different developmental stages simultaneously, thereby increasing reproductive output in resource-variable habitats.[91]
Amphibians
Internal fertilization occurs in a minority of amphibian species, estimated at around 10%, with all caecilians (Gymnophiona, comprising about 3% of amphibians) and over 90% of salamanders (Caudata, about 9% of amphibians) employing this mode, while the vast majority of frogs (Anura, roughly 88% of amphibians) rely on external fertilization.[92][93][94] In salamanders, sperm transfer typically involves indirect methods, such as the male depositing a spermatophore—a gelatinous packet containing sperm—on the substrate during courtship, which the female then takes up via her cloaca; this is particularly characteristic of plethodontid salamanders, the largest family within the order.[95] Some salamander species, such as those in the genus Necturus, achieve fertilization through direct cloacal apposition, where the male and female align their cloacas to transfer sperm without a spermatophore.[93] Caecilians, in contrast, use direct copulation facilitated by the male's eversible copulatory organ, the phallodeum, which deposits sperm into the female's cloaca.[96]A distinctive feature of internal fertilization in amphibians is its association with advanced reproductive strategies, particularly in viviparous caecilians, where embryos develop internally within the oviduct and, after depleting their yolk, engage in matrotrophic feeding by scraping and consuming nutrient-rich secretions from the hypertrophied maternal skin or oviduct lining using specialized fetal dentition.[97] This skin-feeding mechanism provides essential lipids and proteins, enabling prolonged gestation and the birth of well-developed young.Evolutionarily, internal fertilization in amphibians represents a transitional adaptation that supports terrestrial reproduction by protecting gametes from desiccation and predators, as exemplified by the viviparous Alpine salamander (Salamandra atra), which mates on land, retains embryos internally for 2–3 years, and gives birth to live juveniles fully adapted to alpine environments.[98] This mode contrasts with the ancestral external fertilization typical of aquatic-breeding amphibians and underscores the selective pressures for independence from water in higher latitudes or elevations.[98]
Reptiles
Internal fertilization is a universal reproductive strategy among all extant reptiles, enabling the deposition of sperm directly into the female's reproductive tract prior to egg shell formation, a key adaptation for terrestrial reproduction in amniotes. This mode arose as a synapomorphy of the Amniota clade during the late Carboniferous period, approximately 312 million years ago, and became obligatory by the Permian as reptiles diversified on land.[99] In most reptiles, including squamates (lizards and snakes), males possess paired hemipenes—evertible organs stored in the tail base—that are alternately used during copulation to transfer sperm into the female's cloaca. Turtles and crocodilians employ a single penis for intromission, while the tuatara (Sphenodon punctatus) achieves fertilization through cloacal apposition without an intromittent organ.[100] These mechanisms ensure efficient sperm delivery in diverse habitats, from aquatic to fully terrestrial environments.[4]Reptiles exhibit varied post-fertilization strategies, predominantly oviparity but with significant viviparity in about 20% of squamate species. Oviparous reptiles, such as most turtles, lay shelled amniotic eggs that are buried in soil or sand to protect against desiccation and predation; for instance, female sea turtles return to beaches to excavate nests for egg deposition. In contrast, viviparous species like certain boas (e.g., Boa constrictor) retain eggs internally, with embryos receiving supplemental nutrition via a simple placenta that facilitates gas exchange and nutrient transfer beyond yolk reserves. This placental adaptation enhances offspring survival in unstable environments, such as cold or predator-rich areas, and has evolved independently over 100 times within squamates.[101] Viviparity is rare or absent in other reptilian orders, highlighting squamates' reproductive plasticity.[102]A notable feature of reptilian reproduction is long-term sperm storage by females, particularly in turtles, where spermatozoa remain viable in specialized oviductal glands for extended periods. These glands, located in the posterior oviduct, form tubules that nourish and protect sperm, allowing fertilization of eggs laid years after mating; durations up to four years have been documented in species like the box turtle (Terrapene carolina). This adaptation enables females to mate opportunistically and produce multiple clutches from a single insemination, optimizing reproductive success in seasonal or sparse mating opportunities. Similar but shorter storage occurs in some snakes and lizards.[103]In snakes, hemipenes are often elongate and ornamented with spines or folds, facilitating prolonged insemination during copulation, which can last hours and increase sperm transfer efficiency. For example, in garter snakes (Thamnophis spp.), males use one hemipenis at a time in extended mating bouts, allowing for repeated intromissions that enhance fertilization success amid intense male-male competition. This morphology supports cryptic female choice and post-copulatory selection, contributing to the evolutionary diversity of squamate genitalia.[104]
Birds
In birds, internal fertilization is achieved through a process known as the cloacal kiss, where the male and female press their cloacas together to transfer sperm without the use of an intromittent organ such as a penis, which is absent in most avian species.[105] This brief contact allows semen to be deposited directly into the female's reproductive tract, where fertilization occurs in the upper oviduct shortly after ovulation.[106] The mechanism ensures efficient sperm delivery while minimizing physical trauma, adapting to the birds' lightweight skeletal structure and flight capabilities.Following fertilization, the ovum progresses through the oviduct, where layers of albumen, shell membranes, and a hard calcareous shell are sequentially added in specialized regions like the magnum, isthmus, and shell gland.[107] This results in the formation of an amniotic egg, complete with extraembryonic membranes (amnion, chorion, allantois, and yolk sac) that support embryonic development within a self-contained aquatic environment.[108] Unlike internal gestation in other vertebrates, bird eggs are laid and undergo external incubation by the parents, typically lasting 10–80 days depending on species, which allows for larger yolk reserves to fuel development without maternal nutrient transfer post-laying.[106]Avian females possess specialized adaptations for prolonged fertility, including sperm storage tubules (SSTs) in the uterovaginal junction of the oviduct, where viable sperm can be retained for up to 2–15 weeks in domestic hens, enabling sequential egg fertilization over extended periods without repeated matings.[42] Polyspermy, the entry of multiple sperm into the egg, is physiologically common in birds but does not typically disrupt development, as only one sperm fuses with the egg nucleus while others degenerate; the avian zona radiata, an inner glycoprotein layer of the vitelline membrane, helps regulate sperm penetration and contributes to blocking excessive polyspermy.[109][110] In species like albatrosses, which form long-term monogamous pairs, this system supports high paternity assurance, with extra-pair fertilizations being rare (less than 5% in wandering albatrosses), reinforcing pair bonds and biparental care for egg incubation and chick rearing.[111]
Mammals
In mammals, internal fertilization is a universal reproductive strategy achieved through copulation, where the male's penis is inserted into the female's vagina to deposit sperm directly into the reproductive tract.[112] This process ensures sperm are transported to the site of fertilization, typically the oviducts (fallopian tubes), where capacitation—a series of biochemical changes—prepares sperm for binding to the egg's zona pellucida.[7] Fertilization occurs when a single sperm penetrates the egg, triggering blocks to polyspermy and initiating embryonic development.[113]Mammals exhibit diverse post-fertilization strategies, reflecting their evolutionary divergence into three major groups: monotremes, marsupials, and eutherians (placental mammals). Monotremes, such as the platypus and echidnas, represent the most basal lineage; they achieve internal fertilization via cloacal copulation but lay leathery eggs after a brief period of internal development, with no placenta formed.[114] Marsupials, like kangaroos and opossums, also undergo internal fertilization followed by a short gestation, but their embryos develop a simple yolk-sac placenta that provides limited nutrient exchange before birth; newborns are born underdeveloped and continue maturing in a pouch.[115] In contrast, eutherians—the largest group, including humans, rodents, and ungulates—feature a more advanced chorioallantoic placenta, which forms from the fusion of chorionic and allantoic membranes with the uterine wall, enabling prolonged internal gestation and extensive maternal-fetal nutrient, gas, and waste exchange.[116]Gestation periods in mammals vary widely depending on body size, metabolic rate, and environmental adaptations, ranging from as short as 21 days in house mice (Mus musculus) to up to 22 months in elephants (Loxodonta africana and Elephas maximus).[117][118] This developmental phase is primarily regulated by progesterone, secreted by the corpus luteum and later the placenta, which maintains uterine quiescence, supports endometrial growth, and prevents premature contractions to ensure fetal viability.[119]A distinctive feature in many mammals is the process of implantation, where the blastocyst adheres to and invades the uterine endometrium, establishing the placental interface; this is hormonally orchestrated by progesterone and estrogen to synchronize maternal and embryonic tissues.[120] Some species exhibit embryonic diapause, a reversible arrest of development at the blastocyst stage, allowing delayed implantation to align birth with favorable conditions; for example, in the European roe deer (Capreolus capreolus), diapause lasts about five months, during which the embryo remains dormant in the uterus until reactivation in late winter.[121]