Sexual selection constitutes an evolutionary mechanism wherein members of one sex select partners from the opposite sex (intersexual selection) and engage in competition with conspecifics of the same sex for reproductive opportunities with the opposite sex (intrasexual selection). These dual selective pressures result in differential reproductive success among individuals within a population. This disparity may arise, for instance, from enhanced attractiveness or the propensity to choose more desirable mates for procreation. Reproductively successful males typically achieve this through frequent copulation and by securing exclusive access to multiple fertile females. Conversely, females optimize their reproductive energy investment by judiciously selecting and mating with superior males.
Sexual selection is a mechanism of evolution in which members of one sex choose mates of the other sex (intersexual selection) to mate with, and compete with members of the same sex for access to members of the opposite sex (intrasexual selection). 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.
The concept was initially conceptualized by Charles Darwin, who posited it as a "second agency" distinct from natural selection, where competition among potential mates could drive speciation. Ronald Fisher provided a mathematical foundation for this theory during the early 20th century. Sexual selection can compel males to undertake considerable exertions to signal their reproductive fitness to females, resulting in sexual dimorphism in secondary sexual characteristics, exemplified by the elaborate plumage of birds-of-paradise and peafowl, or the prominent antlers of deer. In certain species, these roles may be inverted. This phenomenon is attributed to a positive feedback loop termed Fisherian runaway, wherein the inheritance of a preference for a trait in one sex is as crucial as the trait's presence in the other sex for the runaway effect to manifest. While the sexy son hypothesis suggests a female preference for male offspring, Fisher's principle elucidates the prevalence of an approximately 1:1 sex ratio. This evolutionary force is pervasive across the animal kingdom and is also observed in plants and fungi.
Historical Development
Darwin's Initial Postulation
Sexual selection was initially introduced by Charles Darwin in his 1859 publication, On the Origin of Species, and subsequently elaborated upon in The Descent of Man, and Selection in Relation to Sex (1871), as he contended that natural selection alone could not adequately explain specific non-survival adaptations. He famously expressed his perplexity to a colleague, stating, "The sight of a feather in a peacock's tail, whenever I gaze at it, makes me sick!" His framework categorized sexual selection into two primary components: intrasexual competition among males and intersexual female mate choice.
... is contingent not upon a struggle for existence, but rather upon a contest among males for access to females; the outcome for the unsuccessful competitor is not mortality, but rather a reduction or absence of progeny.
... when the males and females of any animal exhibit similar general habits, yet diverge in structure, coloration, or ornamentation, these distinctions have predominantly arisen through sexual selection.
Alfred Russel Wallace, particularly following Darwin's demise, partially contested these perspectives. While acknowledging the potential for sexual selection, he contended that it represented a comparatively minor selective force. Wallace asserted that intrasexual male competitions constituted forms of natural selection, and furthermore, that the 'drab' coloration of the peahen was inherently adaptive as camouflage. He further opined that attributing mate choice to females implied an capacity for aesthetic judgment in animals (e.g., beetles) that were, in his view, too cognitively rudimentary to possess such aesthetic sensibilities.
Darwin's propositions regarding sexual selection encountered skepticism among his contemporaries and were not initially regarded as highly significant until the 1930s, when biologists began to integrate sexual selection as a distinct mode of natural selection. Their prominence in biology has significantly increased only in the 21st century, with the theory now widely recognized as broadly applicable and analogous to natural selection. A decade-long investigation, which experimentally manipulated sexual selection in flour beetles while maintaining other variables constant, demonstrated that sexual selection conferred protection against extinction even upon an inbred population.
The Fisherian Runaway Mechanism
Ronald Fisher, a distinguished English statistician and evolutionary biologist, elaborated his concepts of sexual selection in his seminal 1930 work, The Genetical Theory of Natural Selection. His contributions encompass the sexy son hypothesis, which posits a potential female preference for male offspring, and Fisher's principle, which accounts for the typical near 1:1 sex ratio. The Fisherian runaway mechanism elucidates how sexual selection intensifies the preference for a particular ornamental trait, leading to a co-evolutionary escalation of both the favored trait and the female preference for it within a positive feedback loop. He observed:
The development of male plumage and female sexual preference for these traits must co-evolve. As long as this process remains unhindered by strong counter-selection, its progression will accelerate. Without such constraints, the rate of development would be directly proportional to the existing level of development, leading to an exponential or geometric increase over time. —Ronald Fisher, 1930
This dynamic leads to a significant escalation in both the male's prominent characteristic and the female's preference for it, culminating in pronounced sexual dimorphism until physiological limitations impede further exaggeration. This establishes a positive feedback mechanism, fostering the evolution of elaborate physical attributes in the sex not constrained by reproductive limits. The long-tailed widowbird serves as a quintessential illustration of female mate choice and potential runaway selection. Although males possess elongated tails favored by female selection, female preferences for tail length are even more pronounced, with females exhibiting attraction to tails exceeding naturally occurring lengths. Fisher posited that the genetic basis for female preference for long tails could be inherited alongside the genes responsible for the long tail itself. Consequently, long-tailed widowbird progeny of both genders inherit both genetic predispositions: females manifest their genetic inclination for long tails, while males display the desirable long tail trait.
Richard Dawkins offers a non-mathematical elucidation of the runaway sexual selection phenomenon in his publication, The Blind Watchmaker. Females exhibiting a preference for males with elongated tails typically descend from mothers who selected long-tailed fathers. Consequently, these females inherit both genetic predispositions. This implies a linkage between genes encoding for long tails and those dictating a preference for them. Thus, the preference for long tails and the actual tail length can become correlated, tending to amplify each other. As tail lengths increase, the desirability of longer tails intensifies. Even a minor initial disparity between preference and trait can trigger a rapid escalation in tail lengths. Fisher articulated this by stating:
The exponential component, which constitutes the core of this phenomenon, originates from the rate at which female preference evolves, being directly proportional to the absolute average level of that preference. —Ronald Fisher, 1932
A female widowbird selects the most appealing long-tailed male for mating, ensuring that her male offspring will also be attractive to subsequent generations of females, thus siring numerous progeny carrying her genes. Given that the rate of change in preference is directly proportional to the average preference among females, and considering females' inclination to mate with the most sexually desirable males, an additive effect emerges. This effect, if unconstrained, can lead to exponential increases in a particular preference and its associated desired sexual characteristic.
It is crucial to recognize that the states of relative stability achieved through these or other mechanisms will persist for a considerably longer duration than the evolutionary process itself, during which the ornamental traits develop. In the majority of extant species, the runaway process must have already been curtailed, suggesting that the more remarkable elaborations of sexual plumage result not from a protracted and consistent trajectory of evolutionary advancement, but rather from abrupt bursts of change. —Ronald Fisher, 1930
Following Fisher's foundational conceptualization of the 'runaway' process, Russell Lande and Peter O'Donald have furnished comprehensive mathematical demonstrations delineating the conditions conducive to runaway sexual selection. Concurrently, biologists have expanded upon Darwin's original formulation; Malte Andersson's widely adopted 1994 definition posits that "sexual selection encompasses the disparities in reproduction stemming from individual variations in traits that influence success in mate competition and fertilization." Notwithstanding certain practical complexities for researchers, the principle of sexual selection remains "straightforward."
Contemporary Theoretical Framework
Reproductive Outcomes
An organism's reproductive success is quantified by the quantity and probable fitness of its progeny. Sexual preference often leads to assortative mating, also known as homogamy. The prevailing conditions for sexual discrimination typically involve two factors: (1) the selection of one mate effectively prevents the acceptance of others, and (2) the rejection of a mating offer is likely to be followed by subsequent opportunities, where the potential benefit of mate selection outweighs the risk of no further offers. Bateman's principle posits that the sex investing more significantly in offspring production becomes a finite resource, leading to competition from the other sex. This is exemplified by the substantial nutritional contribution of an egg to a zygote and the restricted reproductive capacity of females. For instance, human females can typically give birth only every ten months, while males can sire multiple offspring within the same timeframe. However, recent research has cast doubt on the universal applicability of Bateman's principle.
Honest Signaling
The handicap principle, proposed by Amotz Zahavi, Russell Lande, and W. D. Hamilton, suggests that a male's survival to and through reproductive age, despite possessing seemingly maladaptive traits, signals his superior overall fitness to females. These handicaps may indicate either immunity or resistance to disease, or superior speed and physical strength that enable the male to overcome challenges posed by the exaggerated trait. Zahavi's contributions stimulated a re-evaluation of the field and the development of several novel theories. In 1984, Hamilton and Marlene Zuk introduced the 'Bright Male' hypothesis, proposing that elaborate male characteristics could function as health indicators by accentuating the impacts of disease and deficiency.
Male Intrasexual Competition
Intrasexual competition among males arises when two individuals of the same species contend for mating opportunities with a female. Sexually dimorphic traits, body size, sex ratio, and social context can all influence the impact of male-male competition on a male's reproductive success and a female's mate selection. Typically, larger males prevail in male-male conflicts. Males often incur significant risks in these conflicts, necessitating that the value of the contested resource sufficiently justifies such hazards. The outcomes of previous encounters, known as winner and loser effects, further modulate male behavior. Furthermore, male-male competition can impede a female's capacity to choose optimal mates, thereby potentially reducing the probability of successful reproduction.
Diverse Theoretical Models
In recent times, the scope of the field has expanded to encompass additional areas of inquiry, not all of which align with Darwin's original definition of sexual selection. A diverse array of models endeavors to connect sexual selection not only to foundational concepts like anisogamy and parental roles but also to mechanisms such as sex ratios (governed by Fisher's principle), parental care, the 'sexy son' hypothesis, sexual conflict, and the highly debated phenomenon of mate choice. Elaborate characteristics, such as the tail of the Montezuma swordtail (Xiphophorus montezumae), which might appear energetically or functionally costly, do not invariably impose a survival burden. This phenomenon may be attributed to the co-evolution of 'compensatory traits' alongside sexually selected features.
Interplay with Natural Selection
Sexual selection may elucidate how characteristics like feathers possessed survival value during their early evolutionary stages. Early proto-birds, including Protarchaeopteryx, exhibited well-developed feathers despite lacking the capacity for flight. While feathers might have initially provided insulation, aiding females in egg incubation, a courtship display involving forelimb feathers and vigorous jumps could have facilitated a relatively seamless transition to flight.
Sexual selection can, in some instances, drive the evolution of traits that contribute to a species' extinction, as historically posited for the colossal antlers of the Irish elk (Megaloceros giganteus), which vanished in Holocene Eurasia (though climate-induced habitat degradation and anthropogenic pressures are currently considered more probable causes). Conversely, it can also promote species divergence, occasionally through intricate modifications in genitalia, leading to the emergence of novel species. Sexual selection frequently interacts synergistically with natural selection to propel speciation.
Sex-Role Reversal
Darwin explored the concept of sex-role reversal in The Descent of Man, positing that females could be subject to selection by male mating partners. Subsequently, Darwin and other researchers documented such reversed sex roles in the barred buttonquail (Turnix suscitator). Similar deviations from typical sexual hierarchy were observed in pipefish (Syngnathinae) and seahorses (Hippocampus), where females typically exhibit greater size, more vibrant coloration, and increased aggression compared to males.
Across Diverse Taxa
Sexual selection is a pervasive evolutionary force among eukaryotes, manifest in plants, fungi, and animals. Following Darwin's foundational insights concerning humans, extensive research has been conducted on insects, spiders, amphibians, squamates, birds, and mammals, uncovering numerous unique behaviors and morphological adaptations.
Within Mammalian Species
Darwin hypothesized that various heritable characteristics observed in human populations, including beards, hairlessness, and steatopygia, arose from sexual selection. Humans exhibit sexual dimorphism, with females often selecting mates based on attributes such as voice pitch, facial morphology, muscularity, and stature.
A prominent example of sexual selection in mammals is the extreme sexual dimorphism observed in elephant seals, where males can be up to six times heavier than females and engage in intense combat for dominance. Victorious males form extensive harems comprising dozens of females; subordinate males may attempt opportunistic copulations with harem females when the dominant male is distracted. This necessitates continuous territorial defense by the harem male, often preventing him from feeding for periods extending up to three months.
Mammals also exhibit instances of sex-role reversal, exemplified by the highly social meerkat, where a larger female maintains dominance within the group, and inter-female competition is evident. The dominant female is responsible for the majority of offspring production, while subordinate females remain non-reproductive and contribute altruistic care to the young.
In Arthropod Species
Sexual selection is prevalent across numerous spider species, manifesting both pre- and post-copulation. Post-copulatory sexual selection encompasses sperm competition and cryptic female choice. Sperm competition arises when the gametes from multiple males vie to fertilize a female's egg. Cryptic female choice, conversely, involves the female's ability to expel a male's sperm either during or subsequent to copulation.
Insects display diverse forms of sexual selection. While female insects commonly provide parental care, as seen in bees, male parental care is observed in belostomatid water bugs. In these species, after fertilization, the male permits the female to affix her eggs to his dorsal surface. He then incubates them until the nymphs emerge, typically 2–4 weeks later. These substantial eggs diminish the male's capacity to fertilize additional females and capture prey, concurrently elevating his susceptibility to predation.
Among fireflies (Lampyridae beetles), males navigate in darkness, emitting species-specific patterns of light flashes, which are reciprocated by receptive females positioned on perches. The chromatic and temporal characteristics of these flashes are crucial for successful female attraction. Sexual selection is also widespread among other beetle species. For instance, in the mealworm beetle, Tenebrio molitor, males release pheromones to entice females for mating. Females subsequently select mates based on factors such as infection status and body mass.
Within Molluscan Phyla
Post-copulatory intersexual selection is evident in Idiosepius paradoxus, commonly known as the Japanese pygmy squid. Males deposit their spermatangia externally on the female's body. The female then physically dislodges spermatangia from males she presumably finds less desirable.
In Amphibians and Reptiles
Many amphibian species exhibit annual breeding seasons characterized by intense male-male competition. Males typically arrive at aquatic breeding sites in large aggregations, producing diverse vocalizations to attract potential mates. In frogs, males with the deepest croaks and most advantageous territories are often considered the fittest, and females' mate selection is, at least partially, influenced by the depth of these vocalizations. This dynamic has contributed to sexual dimorphism, with females being larger than males in 90% of species, and males engaging in combat to secure access to females. Spikethumb frogs, for instance, are believed to utilize their elongated prepollex in male-male competition to defend mating sites. This prepollex, functioning as a rudimentary digit, features a projecting spine that may be employed during these contests, resulting in scars on the heads and forelimbs of rival males.
Snakes employ diverse strategies to secure mates. Ritualistic combat among males, vying for access to females, frequently involves "topping." This behavior, characteristic of most viperids, entails one male coiling around the vertically raised anterior body of a rival, subsequently forcing it downwards. Neck biting is also a common occurrence during these intertwined encounters.
Avian Species
Avian species have developed a broad spectrum of mating behaviors and numerous forms of sexual selection. These encompass intersexual selection, often manifested as female choice, and intrasexual competition, where members of the more prevalent sex contend for mating opportunities. Significant sexual dimorphism is observed in many species, particularly among birds-of-paradise. Across various bird species, females consistently exhibit a preference for males displaying the most vibrant plumage.
Numerous avian species utilize mating calls, with females demonstrating a preference for males whose songs exhibit complexity and variation in amplitude, structure, and frequency. Furthermore, larger males typically produce deeper vocalizations, correlating with enhanced mating success.
Botanical and Fungal Organisms
Flowering plants exhibit numerous secondary sexual characteristics influenced by sexual selection. These include floral symmetry, particularly if pollinators selectively Sexual dimorphisms are also prevalent.
Fungi, despite frequently engaging in asexual reproduction, also appear to utilize sexual selection. Within Basidiomycetes, a male-biased sex ratio suggests the presence of sexual selection. Male-male competition for fertilization has been observed in various fungi, including yeasts. The employment of pheromone signaling by female gametes and conidia implies a mechanism for male choice. Additionally, the significantly accelerated evolution of female-biased genes in fungi indicates the potential for female-female competition.
References
- Richards, Evelleen (2017). Darwin and the Making of Sexual Selection. Chicago: University of Chicago Press. ISBN 978-0-226-43690-6.Source: TORIma Academy Archive