Sexy son hypothesis

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European pied flycatcher Ficedula hypoleuca -Wood of Cree Nature Reserve, Scotland -male-8a.jpg
European pied flycatcher
Ronald Fisher in 1912 RonaldFisher1912.jpg
Ronald Fisher in 1912

The sexy son hypothesis in evolutionary biology and sexual selection, proposed by Patrick J. Weatherhead and Raleigh J. Robertson of Queen's University in Kingston, Ontario in 1979, [1] states that a female's ideal mate choice among potential mates is one whose genes will produce males with the best chance of reproductive success. This implies that other benefits the father can offer the mother or offspring are less relevant than they may appear, including his capacity as a parental caregiver, territory and any nuptial gifts. Fisher's principle means that the sex ratio (except in certain eusocial insects) is always near 1:1 between males and females, yet what matters most are her "sexy sons'" future breeding successes, more likely if they have a promiscuous father, in creating large numbers of offspring carrying copies of her genes. [2] [ clarification needed ] This sexual selection hypothesis has been researched in species such as the European pied flycatcher. [1]

Contents

Context

Female mating preferences are widely recognized as being responsible for the rapid and divergent evolution of male secondary sex characteristics. [3] In 1915, Ronald Fisher wrote: [4]

Granted that while this taste and preference prevails among the females of the species, the males will grow more and more elaborate and beautiful tail feathers, the question must be answered "Why have the females this taste? Of what use is it to the species that they should select this seemingly useless ornament?" The first step to a solution lies in the fact that the success of an animal in the struggle for existence is not measured only by the number of offspring which it produces and rears, but also by the probable success of these offspring. So that in selecting a mate from a number of different competitors, it is important to select that one which is most likely to produce successful children. [4]

In 1976, prior to Weatherhead and Robertson's paper, [1] Richard Dawkins had written in his book The Selfish Gene :

In a society where males compete with each other to be chosen as he-men by females, one of the best things a mother can do for her genes is to make a son who will turn out in his turn to be an attractive he-man. If she can ensure that her son is one of the fortunate few males who wins most of the copulations in the society when he grows up, she will have an enormous number of grandchildren. The result of this is that one of the most desirable qualities a male can have in the eyes of a female is, quite simply, sexual attractiveness itself. [5]

Ronald Fisher's principle, as published in his book The Genetical Theory of Natural Selection , is one of several possible explanations for the highly diverse and often astonishing ornaments of animals. [6] [7] [8] If females choose physically attractive males, they will tend to get physically attractive sons, and, thus more grandchildren, because other choosy females will prefer their attractive, sexy sons. The theory will function regardless of the physical or behavioral trait a female chooses, as long as it is heritable (that is, the trait varies between individuals of the population), because it is possessing the trait that makes males attractive, and not the qualities of the trait in itself. Once a preference becomes established, females choosing males with elaborate secondary sexual traits will produce sons that carry alleles for the trait and produce daughters that carry alleles for the preference, generating genetic coupling that will drive self-reinforcing coevolution of both trait and preference, due to the mating advantage of males with the trait, creating a Fisherian runaway sexy sons process. [8] Similar models have been proposed for postcopulatory female preferences, such as the time at which females removed the male's sperm ampulla after mating. Sexual selection by direct and/or indirect benefits as well as sexual conflict determine the evolution of animal mating systems. [9]

In its original context, the "narrow-sense sexy son hypothesis" of Weatherhead and Robertson refers to mating systems with care from both parents. In these mating systems, females that mate with a polygynous male normally receive less assistance than females mated with a monogamous male, [10] and thus suffer from direct fitness consequences that have to be (at least) compensated for by the breeding successes of their sexy sons. On the other hand, a "broad-sense sexy son hypothesis" encompasses both polygyny and promiscuous mating systems, with and without care from both parents. Alatalo (1998) [11] argues that the costs of any additional choice may be so minor that female choice for honestly signaling males, that is good genes, may evolve even if the indirect benefits on offspring quality are small. A similar argument can be made for the sexy son hypothesis if mates of attractive males do not suffer any direct fitness consequences. [12]

Sexual conflict

Guianan cock-of-the-rock Guianan Cock-of-the-rock (Rupicola rupicola).jpg
Guianan cock-of-the-rock

Sexual conflict refers to the conflicting goals of breeding males and females. It describes the diverging interests of males and females in optimizing their fitness. From the viewpoint of any one partner, the best outcome would be for the partner's mate to care for the young, thus freeing up his or her own resources (e.g., time and energy) that s/he—but typically he—can invest in further sex that may create additional offspring. In polygynous mating systems, sexual conflict means the optimization of male reproductive success by having mated with multiple females, even though the reproductive success of a polygynously mated female is thereby reduced. [12] Such can be the case for the Guianan cock-of-the-rocks, whose male members spend a majority of their time and energy maintaining their plumage and attempting to seek the most matings. Females, on the other hand, spend their time building and maintaining their nest where they will lay their eggs and raise the young.

Good genes theory

"Good genes" theory proposes that females select males seen to have genetic advantages that increase offspring quality. Increased viability of offspring provides compensation for any lower reproductive success that results from their being "picky". The good-gene hypothesis for polyandry proposes that when females encounter better males than their previous mates, they re-mate in order to fertilize their eggs with the better male's sperm. [7]

Dung beetles who have selected mates with better genetics tend to have offspring that survive longer and are more able to reproduce than those that do not pick mates with genetic quality. This suggests that carefully choosing a mate is beneficial. [13]

Another study notes that pronghorn females engage in an obvious and energetically expensive mate sampling process to identify vigorous males. Though each female selects independently, the outcome is that a small proportion of the herd's males sire most young. Offspring of attractive males were more likely to survive to weaning and to age classes as late as 5 years, apparently due to faster growth rates. [14] Because pronghorn males do not have costly ornaments, the authors conclude that female choice for good genes can exist in the absence of obvious sexual selection cues such as elaborate antlers.

The sexy son hypothesis is closely related to the good genes assumption and the Fisherian runaway selection process. Like good genes, the sexy son hypothesis assumes the existence of indirect genetic benefits that are able to compensate for any inferior direct reproductive success (i.e., fewer offspring). The main difference between good genes and the sexy son hypothesis is that the latter assumes an indirect effect due to the attractiveness of the sons, whereas good genes focus on the viability of both sons and daughters. However, "attractiveness" is not narrowly defined, and can refer to every trait that increases a male's probability to become polygynous.

Sperm models

The successful sperm is the one that fuses with the egg. Sperm-egg.jpg
The successful sperm is the one that fuses with the egg.

Good-sperm models predict positive genetic associations between a male's sperm competitiveness and the general viability of his offspring, [7] whereas sexy-sperm models predict that multiple-mating females produce more grandchildren. [15] [16] As with precopulatory processes, postcopulatory models predict that the trait in males that determines fertilization success will become genetically coupled with the mechanism by which females choose the sperm of preferred males. [17]

See also

Related Research Articles

<span class="mw-page-title-main">Sexual selection</span> Mode of natural selection involving the choosing of and competition for mates

Sexual selection is a mechanism of evolution in which members of one biological sex choose mates of the other sex to mate with, and compete with members of the same sex for access to members of the opposite sex. These two forms of selection mean that some individuals have greater reproductive success than others within a population, for example because they are more attractive or prefer more attractive partners to produce offspring. Successful males benefit from frequent mating and monopolizing access to one or more fertile females. Females can maximise the return on the energy they invest in reproduction by selecting and mating with the best males.

<span class="mw-page-title-main">Behavioral ecology</span> Study of the evolutionary basis for animal behavior due to ecological pressures

Behavioral ecology, also spelled behavioural ecology, is the study of the evolutionary basis for animal behavior due to ecological pressures. Behavioral ecology emerged from ethology after Niko Tinbergen outlined four questions to address when studying animal behaviors: What are the proximate causes, ontogeny, survival value, and phylogeny of a behavior?

<span class="mw-page-title-main">Fisherian runaway</span> Sexual selection mechanism

Fisherian runaway or runaway selection is a sexual selection mechanism proposed by the mathematical biologist Ronald Fisher in the early 20th century, to account for the evolution of ostentatious male ornamentation by persistent, directional female choice. An example is the colourful and elaborate peacock plumage compared to the relatively subdued peahen plumage; the costly ornaments, notably the bird's extremely long tail, appear to be incompatible with natural selection. Fisherian runaway can be postulated to include sexually dimorphic phenotypic traits such as behavior expressed by a particular sex.

<span class="mw-page-title-main">Sperm competition</span> Reproductive process

Sperm competition is the competitive process between spermatozoa of two or more different males to fertilize the same egg during sexual reproduction. Competition can occur when females have multiple potential mating partners. Greater choice and variety of mates increases a female's chance to produce more viable offspring. However, multiple mates for a female means each individual male has decreased chances of producing offspring. Sperm competition is an evolutionary pressure on males, and has led to the development of adaptations to increase male's chance of reproductive success. Sperm competition results in a sexual conflict between males and females. Males have evolved several defensive tactics including: mate-guarding, mating plugs, and releasing toxic seminal substances to reduce female re-mating tendencies to cope with sperm competition. Offensive tactics of sperm competition involve direct interference by one male on the reproductive success of another male, for instance by mate guarding or by physically removing another male's sperm prior to mating with a female. For an example, see Gryllus bimaculatus.

<span class="mw-page-title-main">Reproductive success</span> Passing of genes on to the next generation in a way that they too can pass on those genes

Reproductive success is an individual's production of offspring per breeding event or lifetime. This is not limited by the number of offspring produced by one individual, but also the reproductive success of these offspring themselves.

<span class="mw-page-title-main">Psychological adaptation</span> Psychological theory

A psychological adaptation is a functional, cognitive or behavioral trait that benefits an organism in its environment. Psychological adaptations fall under the scope of evolved psychological mechanisms (EPMs), however, EPMs refer to a less restricted set. Psychological adaptations include only the functional traits that increase the fitness of an organism, while EPMs refer to any psychological mechanism that developed through the processes of evolution. These additional EPMs are the by-product traits of a species’ evolutionary development, as well as the vestigial traits that no longer benefit the species’ fitness. It can be difficult to tell whether a trait is vestigial or not, so some literature is more lenient and refers to vestigial traits as adaptations, even though they may no longer have adaptive functionality. For example, xenophobic attitudes and behaviors, some have claimed, appear to have certain EPM influences relating to disease aversion, however, in many environments these behaviors will have a detrimental effect on a person's fitness. The principles of psychological adaptation rely on Darwin's theory of evolution and are important to the fields of evolutionary psychology, biology, and cognitive science.

<span class="mw-page-title-main">Sexual conflict</span> Term in evolutionary biology

Sexual conflict or sexual antagonism occurs when the two sexes have conflicting optimal fitness strategies concerning reproduction, particularly over the mode and frequency of mating, potentially leading to an evolutionary arms race between males and females. In one example, males may benefit from multiple matings, while multiple matings may harm or endanger females due to the anatomical differences of that species. Sexual conflict underlies the evolutionary distinction between male and female.

<span class="mw-page-title-main">Mate choice</span> Mechanism for evolution

Mate choice is one of the primary mechanisms under which evolution can occur. It is characterized by a "selective response by animals to particular stimuli" which can be observed as behavior. In other words, before an animal engages with a potential mate, they first evaluate various aspects of that mate which are indicative of quality—such as the resources or phenotypes they have—and evaluate whether or not those particular trait(s) are somehow beneficial to them. The evaluation will then incur a response of some sort.

<span class="mw-page-title-main">Lek paradox</span> Conundrum in sexual selection behaviour

The lek paradox is a conundrum in evolutionary biology that addresses the persistence of genetic variation in male traits within lek mating systems, despite strong sexual selection through female choice. This paradox arises from the expectation that consistent female preference for particular male traits should erode genetic diversity, theoretically leading to a loss of the benefits of choice. The lek paradox challenges our understanding of how genetic variation is maintained in populations subject to intense sexual selection, particularly in species where males provide only genes to their offspring. Several hypotheses have been proposed to resolve this paradox, including the handicap principle, condition-dependent trait expression, and parasite resistance models.

A biological ornament is a characteristic of an animal that appears to serve a decorative function rather than a utilitarian function. Many are secondary sexual characteristics, and others appear on young birds during the period when they are dependent on being fed by their parents. Ornaments are used in displays to attract mates, which may lead to the evolutionary process known as sexual selection. An animal may shake, lengthen, or spread out its ornament in order to get the attention of the opposite sex, which will in turn choose the most attractive one with which to mate. Ornaments are most often observed in males, and choosing an extravagantly ornamented male benefits females as the genes that produce the ornament will be passed on to her offspring, increasing their own reproductive fitness. As Ronald Fisher noted, the male offspring will inherit the ornament while the female offspring will inherit the preference for said ornament, which can lead to a positive feedback loop known as a Fisherian runaway. These structures serve as cues to animal sexual behaviour, that is, they are sensory signals that affect mating responses. Therefore, ornamental traits are often selected by mate choice.

Interlocus sexual conflict is a type of sexual conflict that occurs through the interaction of a set of antagonistic alleles at two or more different loci, or the location of a gene on a chromosome, in males and females, resulting in the deviation of either or both sexes from the fitness optima for the traits. A co-evolutionary arms race is established between the sexes in which either sex evolves a set of antagonistic adaptations that is detrimental to the fitness of the other sex. The potential for reproductive success in one organism is strengthened while the fitness of the opposite sex is weakened. Interlocus sexual conflict can arise due to aspects of male–female interactions such as mating frequency, fertilization, relative parental effort, female remating behavior, and female reproductive rate.

Evolutionary aesthetics refers to evolutionary psychology theories in which the basic aesthetic preferences of Homo sapiens are argued to have evolved in order to enhance survival and reproductive success.

Polygyny is a mating system in which one male lives and mates with multiple females but each female only mates with a single male. Systems where several females mate with several males are defined either as promiscuity or polygynandry. Lek mating is frequently regarded as a form of polygyny, because one male mates with many females, but lek-based mating systems differ in that the male has no attachment to the females with whom he mates, and that mating females lack attachment to one another.

<span class="mw-page-title-main">Sexual selection in birds</span> Various types of avian mating rituals/behaviors found in nature

Sexual selection in birds concerns how birds have evolved a variety of mating behaviors, with the peacock tail being perhaps the most famous example of sexual selection and the Fisherian runaway. Commonly occurring sexual dimorphisms such as size and color differences are energetically costly attributes that signal competitive breeding situations. Many types of avian sexual selection have been identified; intersexual selection, also known as female choice; and intrasexual competition, where individuals of the more abundant sex compete with each other for the privilege to mate. Sexually selected traits often evolve to become more pronounced in competitive breeding situations until the trait begins to limit the individual's fitness. Conflicts between an individual fitness and signaling adaptations ensure that sexually selected ornaments such as plumage coloration and courtship behavior are "honest" traits. Signals must be costly to ensure that only good-quality individuals can present these exaggerated sexual ornaments and behaviors.

<span class="mw-page-title-main">Sexual selection in scaled reptiles</span>

Sexual selection in scaled reptiles studies how sexual selection manifests in snakes and lizards, which constitute the order Squamata of reptiles. Each of the over three thousand snakes use different tactics in acquiring mates. Ritual combat between males for the females they want to mate with includes topping, a behavior exhibited by most viperids in which one male will twist around the vertically elevated fore body of its opponent and forcing it downward. It is common for neck biting to occur while the snakes are entwined.

<span class="mw-page-title-main">Sexual selection in amphibians</span> Choice of and competition for mates

Sexual selection in amphibians involves sexual selection processes in amphibians, including frogs, salamanders and newts. Prolonged breeders, the majority of frog species, have breeding seasons at regular intervals where male-male competition occurs with males arriving at the waters edge first in large number and producing a wide range of vocalizations, with variations in depth of calls the speed of calls and other complex behaviours to attract mates. The fittest males will have the deepest croaks and the best territories, with females making their mate choices at least partly based on the males depth of croaking. This has led to sexual dimorphism, with females being larger than males in 90% of species, males in 10% and males fighting for groups of females.

<span class="mw-page-title-main">Polyandry in animals</span> Class of mating system in non-human species

In behavioral ecology, polyandry is a class of mating system where one female mates with several males in a breeding season. Polyandry is often compared to the polygyny system based on the cost and benefits incurred by members of each sex. Polygyny is where one male mates with several females in a breeding season . A common example of polyandrous mating can be found in the field cricket of the invertebrate order Orthoptera. Polyandrous behavior is also prominent in many other insect species, including the red flour beetle, the adzuki bean weevil, and the species of spider Stegodyphus lineatus. Polyandry also occurs in some primates such as marmosets, mammal groups, the marsupial genus' Antechinus and bandicoots, around 1% of all bird species, such as jacanas and dunnocks, insects such as honeybees, and fish such as pipefish.

<span class="mw-page-title-main">Extended female sexuality</span>

Extended female sexuality is where the female of a species mates despite being infertile. In most species, the female only engages in copulation when she is fertile. However, extended sexuality has been documented in Old World primates, pair bonded birds and some insects. Extended sexuality is most prominent in human females who exhibit no change in copulation rate across the ovarian cycle.

The ovulatory shift hypothesis holds that women experience evolutionarily adaptive changes in subconscious thoughts and behaviors related to mating during different parts of the ovulatory cycle. It suggests that what women want, in terms of men, changes throughout the menstrual cycle. Two meta-analyses published in 2014 reached opposing conclusions on whether the existing evidence was robust enough to support the prediction that women's mate preferences change across the cycle. A newer 2018 review does not show women changing the type of men they desire at different times in their fertility cycle.

In humans, males and females differ in their strategies to acquire mates and focus on certain qualities. There are two main categories of strategies that both sexes utilize: short-term and long-term. Human mate choice, an aspect of sexual selection in humans, depends on a variety of factors, such as ecology, demography, access to resources, rank/social standing, genes, and parasite stress.

References

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