Every animal that reproduces sexually has the same job: bringing one sperm and one egg together. A coral, a duck and a mantis all face it, but their routes differ enormously, from mating inside the body to releasing eggs and sperm into the sea on cue from the moon. Much of the strangeness comes from a quiet tug-of-war, because what is best for a male is often not what is best for the female. That is why some of the most dramatic choices happen after mating, out of sight, inside the female’s body.
How Animals Attract and Choose a Mate
Scent is one of the oldest mating signals. Many animals find and recognize mates through pheromones, which are scent signals released by special glands.1PubMed Central. Chemical communication and its role in sexual selection across Animalia These glands are best known in insects and mammals, but they also turn up in fish, birds, frogs, reptiles, centipedes and even flatworms.2PubMed Central. Chemical communication and its role in sexual selection across Animalia
Females are usually the choosier sex, and the reason is in the eggs. Eggs are large and few, while sperm are small and plentiful, so a poor mating choice costs a female more of her reproductive output. That pushes males to display, compete or bribe. There are exceptions, but this is the common pattern.
Bribes can be literal. In some spiders the male catches an insect and wraps it in silk, then presents it as the female approaches. She feeds while he mates. The gift pays off because it lets him mate for longer, so she stores more of his sperm.3PubMed Central. Worthless and Nutritive Nuptial Gifts: Mating Duration, Sperm Stored and Potential Female Decisions in Spiders Some males cheat by wrapping a husk or a bit of plant instead of food.4PubMed Central. Worthless donations: male deception and female counter play in a nuptial gift-giving spider Worthless gifts did not clearly harm females, but females given no gift at all had fewer eggs hatch.5PubMed Central. Worthless donations: male deception and female counter play in a nuptial gift-giving spider What seems to count is that a gift is offered, not what is inside it.6PubMed Central. Worthless donations: male deception and female counter play in a nuptial gift-giving spider
Sound and sight work as signals too. Frogs and crickets call to draw females, and birds use song and display. Females tend to approach the most attractive calls, which sets up the cheater tactics that come later.
Inside or Outside the Body
Many corals release eggs and sperm into the sea all at once, usually several days after a full moon, once a year.7PubMed Central. Moonrise timing is key for synchronized spawning in coral Dipsastraea speciosa Rising sea temperature ripens the eggs and sperm, while the moon sets the exact night.8eLife. Signaling cascades and the importance of moonlight in coral broadcast mass spawning Spawning also tends to fall on calmer tides, which keep the eggs and sperm from being diluted.9eLife. Signaling cascades and the importance of moonlight in coral broadcast mass spawning The trigger itself is a stretch of darkness between sunset and moonrise, which appears after the full moon as the moon rises later.10PubMed Central. Moonrise timing is key for synchronized spawning in coral Dipsastraea speciosa Corals shaded from moonlight spawned on a predictable schedule about 5 days later.11PubMed Central. Moonrise timing is key for synchronized spawning in coral Dipsastraea speciosa Corals kept under shifted temperature, sunlight and moonlight spawned six months out of season.12PubMed Central. Controlled out-of-season spawning of reef-forming corals using offset environmental cues The precision matters because sperm spread out and die fast in seawater, and partners can’t find each other directly.
Inside the body, the female’s tract does much of the moving. People picture sperm racing alone to the egg, but in mammals sperm move through the uterus mostly by riding fluid pushed by muscle contractions, not by swimming.13PubMed Central. Sperm in the Mammalian Female Reproductive Tract: Surfing Through the Tract to Try to Beat the Odds Contractions toward the ovary are strongest when the female is in heat.14PubMed Central. Sperm in the Mammalian Female Reproductive Tract: Surfing Through the Tract to Try to Beat the Odds In rabbits, mating itself sets off strong contractions that carry sperm up the tract.15PubMed Central. Co-Adaptation of Physical Attributes of the Mammalian Female Reproductive Tract and Sperm to Facilitate Fertilization Swimming matters most in the last stretch: near the egg, sperm turn to face the current and swim upstream against it.16PubMed Central. Co-Adaptation of Physical Attributes of the Mammalian Female Reproductive Tract and Sperm to Facilitate Fertilization
Why Genitals Are So Strange
Ducks are one of the clearest examples of how strange genitals can get. Male ducks have long, corkscrew-shaped penises that unfold explosively. In waterfowl species with longer penises, females have longer vaginas with more pouches and spirals.17PubMed Central. Coevolution of Male and Female Genital Morphology in Waterfowl The twists help keep the penis out during forced matings, so the two shapes coevolved through conflict between the sexes.18PubMed Central. Explosive eversion and functional morphology of the duck penis supports sexual conflict in waterfowl genitalia
The female anatomy is cleverly built. The vagina spirals the opposite way to the penis, and dead-end pouches can trap a misdirected one. A willing female can relax to allow entry. As a result, forced matings rarely lead to fertilization. Each side’s adaptations push back on the other, an arms race between the sexes that explains shapes that seem pointlessly complex.
Genitals may also steer which sperm get used. Male genitals may work to push a female into using more of his sperm, even against her interests.19Biological Journal of the Linnean Society. The evolution of animal genitalia: distinguishing between hypotheses by single species studies
Cannibals and Stabbers The Most Extreme Mating
Female praying mantises often eat males during or after mating.20Australian Geographic. Sexual cannibalism could benefit male praying mantis Material from the eaten male’s body ends up in the eggs he fertilized.21PubMed Central. Sexual cannibalism increases male material investment in offspring: quantifying terminal reproductive effort in a praying mantis Females that ate their mates laid on average 51 more eggs, up to 25% more than a usual clutch.22Australian Geographic. Sexual cannibalism could benefit male praying mantis This pays off when a male is unlikely to mate again anyway.23Evolutionary Ecology. The Evolution of Sexual Cannibalism
That doesn’t mean every mating ends in a meal. Many males survive and mate again, and hungry females are more likely to attack. Some spiders and scorpions also eat their mates, though less often.
Bed bugs mate by stabbing. Males pierce the female’s abdomen and inject sperm straight into her body.24PubMed. Traumatic insemination and sexual conflict in the bed bug Cimex lectularius Frequent mating shortened females’ lives and reduced their breeding success.25PubMed. Traumatic insemination and sexual conflict in the bed bug Cimex lectularius Females, though, have a special pad that takes the wounds.26PubMed Central. Costly traumatic insemination and a female counter-adaptation in bed bugs. Piercing outside the pad cut egg output by 50%, while piercing the pad caused no harm.27PubMed Central. Costly traumatic insemination and a female counter-adaptation in bed bugs.
The Race Between Rival Sperm
When females mate with several males, their sperm compete for the eggs. This is called sperm competition.28PubMed. Spermatozoal traits and sperm competition in Atlantic salmon: relative sperm velocity is the primary determinant of fertilization success In Atlantic salmon the fastest sperm won, not the most numerous or longest-lived.29PubMed. Spermatozoal traits and sperm competition in Atlantic salmon: relative sperm velocity is the primary determinant of fertilization success In rodents, competition has reshaped a sperm protein in ways that make sperm swim faster.30PubMed Central. Structural evolution of CatSper1 in rodents is influenced by sperm competition, with effects on sperm swimming velocity In bed bugs the last male to mate fathers most young.31PubMed. Traumatic insemination and sexual conflict in the bed bug Cimex lectularius
Species with intense competition leave clues. Males tend to have large testes for their body size, and females mate with many partners. Sperm are faster or more numerous.
How Females Choose After Mating
Females can influence fatherhood after mating.32PubMed Central. Postmating Female Control: 20 Years of Cryptic Female Choice They may control the timing and order of matings.33PubMed Central. Postmating Female Control: 20 Years of Cryptic Female Choice Some eject, digest or disable part of the sperm they receive.34PubMed Central. Postmating Female Control: 20 Years of Cryptic Female Choice In red garter snakes, female muscle contractions move sperm along.35PubMed Central. Postmating Female Control: 20 Years of Cryptic Female Choice This control is hard to see because it happens inside the body after mating.
Choices can also favour better partners. Fluid released with fish eggs reduced the advantage of males that simply produce more sperm.36PubMed Central. Ovarian fluid allows directional cryptic female choice despite external fertilization In one study, eggs held fewer sperm after a female mated with a related male than with an unrelated one.37PubMed Central. Cryptic female choice favours sperm from major histocompatibility complex-dissimilar males This suggests female bodies may favour genetically different males, which may help offspring health.
The Final Moment Sperm Meets Egg
Eggs release chemicals that sperm follow, steering toward them.38PubMed. Mechanisms of sperm chemotaxis In red abalone this chemical trail effectively doubles the egg’s target size and raises fertilization.39PubMed Central. The ecological and evolutionary consequences of sperm chemoattraction How this works in mammals is still debated.40PubMed. Mechanisms of sperm chemotaxis
Once a sperm reaches the egg’s outer coat, touching it makes the sperm tip release its contents and expose its fusing membrane.41PubMed. Processes controlling sperm-egg fusion In mammals a sperm protein called Izumo binds tightly to an egg protein called Juno, sticking them together.42PubMed Central. The cell biology of fertilization: Gamete attachment and fusion The membranes then fuse and the sperm’s DNA enters.
Scientists care about Izumo and Juno because mice without either protein cannot fertilize. They help explain some unexplained infertility and may inspire future contraceptives.
More than one sperm entering an egg is usually fatal to the embryo, so eggs block extras. In frogs, fertilization quickly changes the egg’s electrical charge, which repels other sperm.43PubMed Central. Ion channels and signaling pathways used in the fast polyspermy block The flip happens within seconds. In lampreys a slower, permanent barrier forms as a fluid-filled gap opens around the egg.44Journal of Experimental Zoology. Fertilization of the lamprey (<i>Lampetra japonica</i>) eggs: Implication of the presence of fast and permanent blocks against polyspermy
Cheaters, Hermaphrodites and Virgin Births
Males with less attractive calls, or none at all, often lurk near calling males to intercept females.45Animal Behaviour. Intersexual dynamics mediate the expression of satellite mating tactics: unattractive males and parallel preferences In one cricket, 36.6% of normal-wing males used this lurking tactic versus 12.7% of silent flatwing males.46PubMed Central. Divergent alternative mating tactics in convergent male reproductive morphs Which tactic wins depends on conditions such as predation risk.47bioRxiv. A Theoretical Comparison of Alternative Male Mating Strategies in Cephalopods and Fishes Cheaters persist because they avoid costly fights and displays, and females sometimes still choose them.
Some animals are both sexes. In one flatworm with both sexes, partners inject each other with sperm at the same time.48Animal Behaviour. Sexual selection in a simultaneous hermaphrodite with hypodermic insemination: body size, allocation to sexual roles and paternity Animals struggle to break away when they can’t donate sperm in return.49Animal Behaviour. Sexual selection in a simultaneous hermaphrodite with hypodermic insemination: body size, allocation to sexual roles and paternity
Some females can reproduce without a male. It has been confirmed in sharks, king cobras and a crocodile.50PubMed Central. Genome-wide data implicate terminal fusion automixis in king cobra facultative parthenogenesis51PubMed Central. Discovery of facultative parthenogenesis in a new world crocodile Offspring carry much less genetic variety than normal, keeping only about a quarter of the mother’s mix in king cobras.52PubMed Central. Genome-wide data implicate terminal fusion automixis in king cobra facultative parthenogenesis
Hormones, Microbes and the Hidden Influence on Mating
Hormones flip the switch for readiness. In female rats estrogen and then progesterone together turn on sexual receptivity.53PubMed Central. Neural and Hormonal Control of Sexual Behavior In fruit flies a rise in a growth hormone switches receptivity on.54Animal Behaviour. The control of sexual receptivity in female Drosophila
Microbes in the reproductive tract can affect fertility through hormones, immunity and sperm movement.55PubMed Central. Special series on the role of the microbiome in reproduction and fertility In wild animals microbes play roles from mate attraction to birth.56PubMed Central. Connecting microbial ecology to human fertility and reproduction: perspectives from the reproductive microbiomes of animals
Genes join in too. In mammals some genes act differently depending on which parent they came from.57Population Ecology. Conflict theory of genomic imprinting in mammals Father’s genes tend to push the fetus to take more from the mother, while mother’s genes hold back.58PubMed. The conflict theory of genomic imprinting: how much can be explained? This is the same male-female tension, now playing out in the embryo.