Matt Ridley on the Evolution and Biology of Sex

Mating Systems 101

In a monogamous mating system, consistent pair bonds are formed between two individuals with sexual exclusivity. Polygamy is a general term used to describe a system in which an individual mates with 2 or more partners of the opposite sex. Two subsets exist within this definition. In a polygynous system, one male mates with two or more females. In a polyandrous system, one female mates with two or more males.

Polygynandry is a mating system defined by the sexual sharing among two or more females and two or more males. This term is often used interchangeably with promiscuity, but it differs because pair bonds form among specific individuals. In a promiscuous regime, no pair bonds are formed.

Across the board, mating systems develop to optimize the reproductive success of individuals. Monogamy will prevail when it is most fitness enhancing for those involved. For example, if females are dispersed, which is the case in some mammal and many bird species, monogamy will likely be the dominant strategy observed. If females are forced into a small area, such as female elephant seals cramped along a shoreline, males will use the opportunity to sequester females and maximize their reproductive output.

Monogamy will also prevail if the fitness of the offspring is dependent upon biparental care. In many bird species, the male and female are both fully capable of incubating the eggs and feeding hatchlings. If only one parent is involved, the probability of the chicks’ survival is compromised. Female-enforced monogamy is when a female eliminates the risk of other competing females from copulating with her chosen mate. A deep-sea angler fish male is born as a small, helpless sperm packet who lacks a digestive system and is entirely dependent upon his destine host female. He swims though the deep ocean in search of her, and has specialized mouth parts that assist in him in his permanent attachment to her.

Polygyny is by far the most commonly observed mating system in Animalia, and its presence is based on the extent to which males can monopolize females. This model applies to species in which the territory of a male contains useful resources for the female and her offspring. The environment plays a significant role in this mating system because females are easier to sequester when resources are spatially clumped. For example, female elephant seals in the Falkland Islands typically rear offspring and feed along the shoreline. Males fight one another in an effort to establish a more dominant hierarchy ranking which allows them access to the largest territory of shoreline. Once established, he is considered a harem holder, and mates with all the females who nest in his territory (a heram group). In polygynous mating systems, male reproductive success is a function of pre-copulatory strategies such as fighting in the example above. Males aim to mate with as females as possible, and females choose the male based on the quality of the territory he protects. A very small percentage of alpha males are successful harem holders among polygynous populations. The remaining male elephant seals roam the periphery of the territories, and are called satellite males.

Polyandry has been considered an evolutionary problem because it was thought to challenge one of the major underpinnings of sexual selection. It is the assumption that the disparity between male and female gamete investments (anisogamy) has favored the selection for diverging mating habits between males and females. Females are thought to be the “choosier” sex because they invest more energy into generating eggs, while males tend to favor quantity over quality and their fitness will not be lowered if they mate with a female of low genetic quality.

This line of thinking has gone under extreme scrutiny recently, as there has been accumulating molecular evidence revealing multiple paternity (polyandry) to be a common practice in animals. Multiple hypotheses have developed to explain this. The material benefits hypothesis predicts females who mate with more than one male are privileged to access more resources, parental care, and a limitless sperm supply. The genetic benefits hypothesis broadly predicts females who are mated with multiple males will produce offspring who are the result of superior ejaculates. If the offspring are males, they potentially have the same high quality sperm and will be able to heighten the fitness of the mother.

There are unique cases that do not fit in the categories described above. For example, we see an investment role reversal in Red Phalaropes of Alaska. Females exhibit traditionally masculine qualities. They are bigger and more colorful than males and play no role in incubating or caring for the young. The female spends about a week courting a single male and laying her eggs in his nest. Females of this species are able to generate eggs quickly, and after a week the female begins searching for another mate. Males incubate the eggs and nurture the chicks alone.

Polygynandry and promiscuity are similar yet distinctly different mating systems. Polygynandrous females regularly form pair bonds and copulate with several males at the same time as males form pair bonds and copulate with several females. The polygynandrous European badger lives in social groups with as many as five mothers and five fathers that produce multiple-paternity litters. It is thought the primary reason for this is described by the resource dispersion hypothesis: polygynandrous groups may arise because limited optimal resources may force more than one breeding pair within a territory. There is usually a dominant pair and a number of subordinates within a social group. In some species the subordinates do not mate, but in many cases subordinate females produce litters of mixed paternity.

Promiscuous species are those in which pair bonds do not form and males and females are likely to copulate with more than one individual of the opposite sex. It is a unique system because subordinate males have the opportunity to access females and male reproductive success is a function of post-copulatory strategies such as sperm competition and cryptic female choice. For example, when brown headed cowbirds live in areas with abundant resources, territorial lines are not well defined and promiscuity is often reported. The brown headed cowbird is a nest parasite that lays its eggs in other birds’ nests and provides no parental care for its young. Promiscuity may be the obvious choice given the birds’ behaviors and their lack of parental care.

Traumatic Insemination in aptly named 'Harpactea sadistica' spider

A violent but evolutionarily effective mating strategy has been spotted in spiders from Israel. Males of the aptly-named Harpactea sadistica species pierce the abdomen of females, fertilising their eggs directly in the ovaries. This has been described as a "traumatic insemination strategy," in which insemination wounds are created by male genitalia in areas outside the genital orifice of females. It is practiced because it gives the first male a reproductive advantage by bypassing structures in the females' genitalia.

These tactics have been observed in insects such as mites, bedbugs, and flies, but this study was the first time that it was documented in spiders. Typically, spider males deliver their genetic package via sperm that manually inserted using a pair of appendages called pedipalps.

The sperm are then held in a receptacle between the ovipore and ovary known as a spermatheca until an egg is released. However, the spermatheca is a "last in, first out" structure, so that if any further males inseminate a female, the last mate's sperm is the first in line to fertilize an egg.

Milan Rezic, an entomologist at the Crop Research Institute in Prague, has spotted a spider circumventing this problem by delivering sperm directly to the ovaries via holes that the males bore directly in the females' abdomens. The male possesses a pair of emboli, appendages modified for piercing females.

The way in which the male H. sadistica inseminates the female is choreographed and complex. The male taps the female, subdues her, and wraps himself around her to properly position the sex organs. He then alternates between the two organs, piercing and injecting the sperm on one side, then the other. The physical marks left are two neat rows of holes in her abdomen.

An analysis of the females of the species has shown that relative to other spiders, their spermathecae are atrophied, or shrunken. In an apparent case of co-evolution, they seem to be slowly shrinking into nonexistence now that their purpose is being bypassed by the males' more direct approach. This is yet another example of the co-evolutionary arm's race we see between many male and female species, in which males evolve to more efficiently inseminate the female and displace other males' seminal fluid, and females evolve to be able to control who inseminates her precious eggs.

Dr. Rezac foresees the race continuing. He suggests that a means to avoid the injury caused by the males might drive the evolution of secondary genitalia nearer to the ovaries, which have been observed in some spiders and butterflies.

Rezac, M. 2009. The spider Harpactea sadistica: co-evolution of traumatic insemination and complex female genital morphology in spiders. Proceedings of the Royal Society: Biological Sciences 276(1668):2697-701.