Geographic distribution of human skin colour: A selective compromise between natural selection and sexual selection?

Modern humans have been shaped by the cumulative action of natural selection, non-adaptive random change, and sexual selection. The last of these is not universal and has prevailed in one of two circumstances: (1) A surplus of females due to high male mortality, combined with ecological constraints on female participation in food procurement which discourage males from taking second wives; (2) A surplus of single males due to generalized polygyny with relatively low male mortality. These circumstances are most likely to occur in (1) Arctic tundra environments, specifically the vast expanse of tundra covering most of Europe up to 10,000 B.P., and in (2) regions dominated by generalized polygyny, notably sub-Saharan Africa. Sexual selection often acts on existing sex differences, including perhaps sexual dimorphism in human skin colour. Whereas women are universally fairer in complexion, men are browner and ruddier; parallel to this, most human societies see lighter skin as more feminine and darker skin as more masculine. Hence, sexual selection should favour lighter pigmented women when a surplus of single females must compete for a mate. Since skin colour is only mildly sex-linked, both sexes would lighten in pigmentation within the population in question. Similarly, when a surplus of single males must compete for a mate, both sexes would darken. Geographic variation in human skin colour may thus represent a selective compromise between two counterbalancing forces: natural selection, as determined by latitudinal variation in sunlight; and sexual selection, as determined by variations in the following: male mortality rates, incidence of polygyny, and ecological constraints on female participation in food procurement.     

The ecological benefits of larger colony size may promote polygyny in ants

How polygyny evolved in social insect societies is a long‐standing question. This phenomenon, which is functionally similar to communal breeding in vertebrates, occurs when several queens come together in the same nest to lay eggs that are raised by workers. As a consequence, polygyny drastically reduces genetic relatedness among nestmates. It has been suggested that the short‐term benefits procured by group living may outweigh the costs of sharing the same nesting site and thus contribute to organisms rearing unrelated individuals. However, tests of this hypothesis are still limited. To examine the evolutionary emergence of polygyny, we reviewed the literature to build a data set containing life‐history traits for 149 Palearctic ant species and combined this data set with a reconstructed phylogeny. We show that monogyny is the ancestral state and that polygyny has evolved secondarily and independently throughout the phylogenetic tree. The occurrence of polygyny is significantly correlated with larger colony size, dependent colony founding and ecological dominance. Although polydomy (when a colony simultaneously uses several connected nests) tends to occur more frequently in polygynous species, this trend is not significant when phylogenetic history is accounted for. Overall, our results indicate that polygyny may have evolved in ants in spite of the reduction in nestmate relatedness because large colony size provides immediate ecological advantages, such as the more efficient use of temporal food resources. We suggest that the competitive context of ant communities may have provided the conditions necessary for the evolution of polygyny in some clades.     

Male versus female mate choice: sexual selection and the evolution of species recognition via reinforcement

Male mate choice, expressed through courtship preferences, sometime occurs even under the mating system of polygyny, when the operational sex ratio is skewed toward males. The conditions under which male mate choice may be expected during polygyny are not well established. Servedio and Lande (2006, Evolution 60:674-685), assuming strict polygyny where all females have equal mating success, show that when having a preference does not increase the amount of energy that a male can put into courtship, male preferences for "arbitrary" female ornaments should not be expected to evolve; direct selection acts against them because they place males that carry them into situations in which there is high competition for mates. Here I explore in detail two situations under which logic dictates that this effect may be overcome or reversed. First I determine the contributions that direct and indirect selection place on male versus female preferences for traits that increase viability, using notation that allows the exact expression of these measures of selection. I find that direct selection against male preferences still predominates in the male mate choice model, causing less evolution by male than female preferences under these conditions. Second I address whether male mate choice is likely to evolve as a mechanism of premating isolation leading to species recognition, driven by the process of reinforcement. Reinforcement is compared under male and female mate choice, using a variety of models analyzed by both analytical techniques assuming weak selection and numerical techniques under broader selective conditions. I demonstrate that although under many conditions stronger premating isolation evolves under female mate choice, reinforcement may indeed occur via male mate choice alone.     

Sexually transmitted diseases in polygynous mating systems: prevalence and impact on reproductive success

Studies of disease in relation to animal mating systems have focused on sexual selection and the evolution of sexual reproduction. Relatively little work has examined other aspects of ecological and evolutionary relationships between host social and sexual behaviour, and dynamics and prevalence of infectious diseases; this is particularly evident with respect to sexually transmitted diseases (STDs). Here, we use a simulation approach to investigate rates of STD spread in host mating systems ranging from permanent monogamy to serial polygyny or polyandry and complete promiscuity. The model assumes that one sex (female) is differentially attracted to the other, such that groups of varying size are formed within which mating and disease transmission occur. The results show that equilibrium disease levels are generally higher in females than males and are a function of variance in male mating success and the likelihood of a female switching groups between mating seasons. Moreover, initial rates of disease spread (determining whether an STD establishes in a population) depend on patterns of host movement between groups, variance in male mating success and host life history (e.g. mortality rates). Male reproductive success can be reduced substantially by a sterilizing STD and this reduction is greater in males that are more 'attractive' to females. In contrast, females that associate with more attractive males have lower absolute fitness than females associating with less attractive males. Thus, the potential for STDs to act as a constraint on directional selection processes leading to polygyny (or polyandry) is likely to depend on the details of mate choice and group dynamics.     

Male–female evolutionary game on mate-locating behaviour and evolution of mating systems in insects

We present a model of a male–female evolutionary game on mate-locating behaviour. Two major mating systems are considered: "lek polygyny" (in which males aggregate to wait for females searching for males) and "searching polygyny" (in which males search for females emerging or waiting for males). The model predicts that lek polygyny is favoured (i) when male survivorship during lekking is sufficiently higher than that during mate searching, (ii) when female survivorship while visiting a lek is sufficiently higher than at the emergence site, or (iii) when searching efficiency is higher at a lek than at an emergence site. Furthermore, the model shows that a reduction in the reproductive value of females later in the day, which prevents males from performing riskier mate-locating behaviour, can result in a change of mating system. In addition, mixed mating systems can be realized as transient states during this shift.     

DISENTANGLING THE CONTRIBUTION OF SEXUAL SELECTION AND ECOLOGY TO THE EVOLUTION OF SIZE DIMORPHISM IN PINNIPEDS

The positive relationship between sexual size dimorphism (SSD) and harem size across pinnipeds is often cited as a textbook example of sexual selection. It assumes that female aggregation selected for large male size via male–male competition. Yet, it is also conceivable that SSD evolved prior to polygyny due to ecological forces. We analyzed 11 life‐history traits in 35 pinniped species to determine their coevolutionary dynamics and infer their most likely evolutionary trajectories contrasting these two hypotheses. We find support for SSD having evolved prior to changes in the mating system, either as a consequence of niche partitioning during aquatic foraging or in combination with sexual selection on males to enforce copulations on females. Only subsequently did polygyny evolve, leading to further coevolution as the strength of sexual selection intensified. Evolutionary sequence analyses suggest a polar origin of pinnipeds and indicate that SSD and polygyny are intrinsically linked to a suite of ecological and life‐history traits. Overall, this study calls for the inclusion of ecological variables when studying sexual selection and argues for caution when assuming causality between coevolving traits. It provides novel insights into the role of sexual selection for the coevolutionary dynamics of SSD and mating system.     

Mating system and reproductive success in eastern Pacific harbour seals

Harbour seals sometimes breed along inland travel corridors where females become clustered in space and time and males establish underwater acoustic display territories similar to terrestrial arenas known as resource-based leks. Under these conditions, we predicted that higher levels of polygyny would be observed than has been previously reported for this species mating in open coast environments without travel corridors. Reproductive success (RS) of 70 males was measured using 20 microsatellite DNA loci and likelihood-based paternity analysis of 136 offspring collected over 3 years. Most males were assigned either zero or one paternity with 80% confidence. The greatest number of pups assigned to one male in a season was two. Variance in RS was higher for males than females (which are biologically limited to one offspring per year) indicating low to mild polygyny. In addition, distributions of relatedness values among pups within year classes did not differ significantly from a simulated distribution with R = 0, indicating that half-siblings were uncommon. Overall, polygyny levels were low relative to terrestrial pinniped mating systems and similar to observations from a harbour seal population along an open coast. Due to large confidence intervals associated with our results, we cannot rule out the hypothesis that a travel corridor might increase the degree of polygyny skew relative to that observed in open coast environments. Habitat appeared to influence male strategies as the most successful males in open coast environments patrolled offshore, while the most successful male in this study defended a territory along the travel corridor.     

Male ornamentation, timing of breeding, and cost of polygyny in the collared flycatcher

Highly ornamented males are often thought to be better ableto provide females with resources, parental assistance, or goodgenes. Individual variation in such male abilities may overridethe costs of polygyny and therefore largely explain within-populationvariation in mating patterns. We investigated the influenceof variation in male ornamentation and the environment on thecosts of polygyny for female collared flycatchers (Ficedulaalbicollis), using data from a long-term study involving 2733breeding attempts over 19 years. We show that females sufferreduced reproductive success when mated polygynously but thatthe costs of polygyny depend on an interaction between maleornamentation and timing of breeding. Among early breeders,polygynously mated females experience higher reproductive successwhen mated to less ornamented males, but among late breeders,females mated polygynously to highly ornamented males were moresuccessful. We suggest that a high effort spent on obtainingextrapair matings early in the season renders highly ornamentedmales less able to assist two females in caring for the young.Thus, a male's ability to simultaneously gain from extrapairmatings and polygyny may be limited through direct effects onfemale reproductive success. Given such limitation, extrapairmatings may be expected to be less frequent in species withbiparental care and a high level of social polygyny.     

A mixed model of the evolution of polygyny and sexual size dimorphism in mammals

The theory of sexual selection is the most widely accepted theory explaining the evolution of mating systems and secondary sexual characters. Polygyny is the most common mating system in mammals, and there is a strong correlation between the degree of polygyny and the degree of sexual size dimorphism skewed towards males. Sexual selection theory posits that polygyny in mammals has evolved through direct, precopulatory, intrasexual selection in males, and that sexual size dimorphism is a result of male competition for mates. New results that are being obtained with the use of molecular techniques and with comparative phylogenetic methods do not appear to support predictions from this classical model in full. In this article, an expansion of the classical model is presented that combines the effects of at least four forms of selection: natural, precopulatory intrasexual, postcopulatory intrasexual, and intersexual selection. This mixed model consists of an initial phase in which natural selection operates on body size, followed by a second phase dominated by sexual selection and involving increases in sexual dimorphism and coercive behaviour of males towards females. Sexual harassment induces female aggregation, thus creating social potential for polygyny. Males compete for access to the groups of females, following two possible evolutionary scenarios, directional or equilibrium sexual selection, both producing similar behavioural polygyny, but with differences in the intensity of intra-male precopulatory sexual selection. Predictions of the mixed model are as follows: 1) polygyny can exist without high variance in male reproductive success (a fundamental requirement in the classical model); 2) extra-group fertilisation can be common; 3) sexual size dimorphism evolved prior to polygyny; 4) sexual coercion is widespread; and 5) females reduce levels of sexual coercion by joining groups.     

Female control of the distribution of paternity in cooperative breeders

Models of reproductive skew have shed light on why animal societies vary in the partitioning of reproduction among group members. However, their application to cooperative vertebrate societies remains controversial. A particular problem is that previous models assume that skew in paternity is determined by interactions among males and males only. This conflicts with observations from many species that indicate that females exert control over the distribution of paternity. Here we address this shortfall in the current theory by developing two models to explore the expected patterns of skew in three member groups in which a female controls the allocation of paternity among two males. The first "staying incentive" model extends previous "transactional" (or "concession") models to examine the conditions where females will be willing to share reproduction among a dominant and a subordinate male to retain the subordinate in the group. The second "work incentive" model explores patterns of skew where females allocate paternity in order to maximize the amount of care their offspring receive. The models make contrasting predictions about the nature of male-female conflict over reproduction and also about the relationships between skew and relatedness, ecological constraints, the relative quality of the subordinate male, and the relative cost of care for the two males. These divergent predictions provide a schema by which the evolutionary causes of variation in skew among males can be evaluated.     

Population consequences of individual heterogeneity in life histories: overcompensation in response to harvesting of alternative reproductive tactics

Alternative reproductive tactics (ARTs) are examples of individual heterogeneity in which males adopt one of typically two alternative strategies to mate with females: males are either large, armed fighters or small, benign sneakers. ART expression is often conditionally determined, and variation in the expression of conditional ARTs due to genetic and/or environmental influences can greatly affect population composition and trajectory. For example, ecological feedback mechanisms resulting from strong density‐dependent competition over food have been suggested to explain the observation that the harvesting of scramblers (= sneakers) in closed populations of the bulb mite Rhizoglyphus robini did not result in an increase (expected from quantitative genetics theory) but decrease in fighter expression. Here, we exposed closed bulb mite populations to selective fighter or scrambler harvesting for 5–6 generations under abundant food (to halt ecological feedbacks through density‐dependence) to confirm predictions from quantitative genetics theory. However, we found no evolutionary shift in ART expression; rather, we observed an overcompensatory ecological response, whereby the number of fighters increased when we harvested them. Treatment effects on scrambler numbers could not be tested as there were too few in the experimental populations. Further experiments revealed that starved fighters preferentially killed immature males and immature fighters; possibly to reduce male‐male competition as e.g. immature fighters have not yet developed their lethal weaponry. If this is so, then harvesting adult fighters reduced the killing pressure on immature males in our experiment, which resulted in an overcompensatory number of immature fighters that matured as adults. Our results highlight the complexity of how individual heterogeneity in ARTs affects the ecological and evolutionary processes that determine population fluctuations.     

Trade up polygyny and breeding synchrony in avian populations

The advent of the molecular techniques used to assign paternity has focused attention on the differences between the social and the genetic mating systems of sexual species. In particular, the interrelations between breeding synchrony-the degree to which the fertility periods of individual females in a population overlap and the degree of extra pair paternity (EPP) in that population, has became a subject of a lively debate. Investigation of the subject can be facilitated by examining the criteria that females use in choosing extra pair partners. These preferences constitute a continuum ranging between two extremes. At one end, there are situations wherein all the females in a population exhibit a preference for males with particular phenotypic markers, and females mated to males lacking such "quality" markers seek extra pair fertilizations from males that do -trade up polygyny. At the other extreme, there are situations wherein females seek to maximize the total number of male partners, rather than secure fertilization by males of particular type -indiscriminate polygyny. Previously, we used game theoretical methods to model the interrelations between breeding synchrony and EPP in the context of indiscriminate polygyny. Here we present an analogous investigation in the context of trade up polygyny. Our results for the two cases, which delimit the range of the possible behavior, are similar. That is, we see that it is the pursuit of extra pair fertilizations opportunities that determines breeding synchrony of populations, rather than the vice versa as has been previously suggested.     

The ecology of sexual selection: Mean crowding of females and resource-defence polygyny

Summary Resource-defence polygyny is a mating system that offers an opportunity for strong sexual selection. I express the degree of aggregation or clustering of females at resources at the time of mating using Lloyd's measures of microspatial aggregation, mean crowding (m ^*) and patchiness (P). Here, I show that Lloyd's two ecological measures of aggregation can be used to quantify the relationship between resource-based polygyny and sexual selection. The advantage of using these measures is that some of the statistical machinery for estimating the degree of mean crowding and testing for density dependence in comparative ecological studies can be applied to estimating the strength of sexual selection and comparing different mating systems. When females vary in their tendency to aggregate with other females and males vary from one another in their ability to guard aggregations of females, a run-away process of sexual selection is possible. The largest aggregations of females have a higher proportion of the females most prone to aggregate or most tolerant of crowding. The males with the highest mating success have daughters more prone to aggregate and sons better at defending aggregated females against other males. As a result, females are selected to over-aggregate with respect to resources. The run-away process halts when single males cannot defend and maintain exclusive reproductive access to clusters of females as evidenced by extraharem copulations and paternity.     

Sperm competition and sex change: a comparative analysis across fishes

Current theory to explain the adaptive significance of sex change over gonochorism predicts that female-first sex change could be adaptive when relative reproductive success increases at a faster rate with body size for males than for females. A faster rate of reproductive gain with body size can occur if larger males are more effective in controlling females and excluding competitors from fertilizations. The most simple consequence of this theoretical scenario, based on sexual allocation theory, is that natural breeding sex ratios are expected to be female biased in female-first sex changers, because average male fecundity will exceed that of females. A second prediction is that the intensity of sperm competition is expected to be lower in female-first sex-changing species because larger males should be able to more completely monopolize females and therefore reduce male-male competition during spawning. Relative testis size has been shown to be an indicator of the level of sperm competition, so we use this metric to examine evolutionary responses to selection from postcopulatory male-male competition. We used data from 116 comparable female-first sex-changing and nonhermaphroditic (gonochoristic) fish species to test these two predictions. In addition to cross-species analyses we also controlled for potential phylogenetic nonindependence by analyzing independent contrasts. As expected, breeding sex ratios were significantly more female biased in female-first sex-changing than nonhermaphroditic taxa. In addition, males in female-first sex changers had significantly smaller relative testis sizes that were one-fifth the size of those of nonhermaphroditic species, revealing a new evolutionary correlate of female-first sex change. These results, which are based on data from a wide range of taxa and across the same body-size range for either mode of reproduction, provide direct empirical support for current evolutionary theories regarding the benefits of female-first sex change.     

The ecology and evolution of male reproductive behaviour in the bees and wasps

Males of aculeate Hymenoptera differ in the behavioural adaptations employed to locate and secure mates. The ecological and evolutionary bases of these differences are explored in this paper. Male bees and wasps search for females by patrolling widely within emergence-nesting areas or within patches of flowers attractive to conspecific females, or by waiting at landmarks, at specific emergence sites, or at nests. Nest dispersion, flower distribution, the type of female mating system and the nature of male-male competition appear to be key factors in determining the mate-locating behaviour of males. Of special interest in multiple-mating by females, which may be an evolutionary response to the costs of attempting to resist copulation in certain situations. When polyandry occurs, males are under selection pressure to be the last male to copulate with a female prior to oviposition if sperm precedence occurs. In species in which females mate just once, a selective premium is placed on being the first male to reach a virgin female. In either case, because receptive females are a limited resource, there is intense competition among males for access to the resource. The density of competitor males may play an important role in determining whether holding a relatively restricted territory is preferable to the strategy of patrolling widely at various sites which may have females. Territoriality is practiced by males of several species of aculeate Hymenoptera when the number of male competitors is relatively few in number and the distribution of emergence sites or foraging areas of females is clumped in space.     

MULTI‐LEVEL SEXUAL SELECTION: INDIVIDUAL AND FAMILY‐LEVEL SELECTION FOR MATING SUCCESS IN A HISTORICAL HUMAN POPULATION

Precopulatory sexual selection is the association between fitness and traits associated with mate acquisition. Although sexual selection is generally recognized to be a powerful evolutionary force, most investigations are limited to characters belonging to individuals. A broader multilevel perspective acknowledges that individual fitness can be affected by aspects of mating success that are characters of groups, such as families. Parental mating success in polygynous or polyandrous human societies may exemplify traits under group‐level sexual selection. Using fitness measures that account for age‐structure, I measure multilevel selection for mate number over 55 years in a human population with declining rates of polygyny. Sexual selection had three components: individual‐level selection for ever‐mating (whether an individual mated) and individual‐ and family‐level selection for polyandry and polygyny. Family‐ and individual‐level selection for polygyny was equally strong, three times stronger than family‐level selection for polyandry and more than an order of magnitude stronger than individual‐level selection for polyandry. However, individual‐level selection for polyandry and polygyny was more effective at explaining relative fitness variance than family‐level selection. Selection for ever‐mating was the most important source of sexual selection for fitness; variation for ever‐mating explained 23% of relative fitness variance.     

Reproductive synchrony in the intertidal amphipod Corophium volutator

Following logic of the mate-availability hypothesis, females are expected to show asynchronous reproduction in those species where operational sex ratios are female-biased and under circumstances where an individual female is sexually receptive only for short durations. We show that females of the intertidal amphipod Corophium volutator are receptive to mating only for a few days following their moult and are unable to hasten onset of moulting in the presence of a male. Despite meeting the conditions of the mate-availability hypothesis, reproduction was synchronous for female C. volutator across spatial and temporal scales relevant to mate-searching abilities of males. As such, some females are not expected to mate between moults, which coincide with their ability to mate. However, females do moult frequently (relative to males) which should increase their likelihood of mating over their lifetimes. It is unlikely that seasonal constraints, predation, or competition can account for the high degree of synchrony among breeding female amphipods. We suggest that dispersal of females or their offspring may constrain activity of females, as they moulted almost entirely during spring tides (although not always during the same set of spring tides). Female reproductive synchrony also has implications for reproductive behaviour of males, in particular, the possibility of harem-defence polygyny.     

Incestuous Sisters: Mate Preference for Brothers over Unrelated Males in Drosophila melanogaster

The literature is full of examples of inbreeding avoidance, while recent mathematical models predict that inbreeding tolerance or even inbreeding preference should be expected under several realistic conditions like e.g. polygyny. We investigated male and female mate preferences with respect to relatedness in the fruit fly D. melanogaster. Experiments offered the choice between a first order relative (full-sibling or parent) and an unrelated individual with the same age and mating history. We found that females significantly preferred mating with their brothers, thus supporting inbreeding preference. Moreover, females did not avoid mating with their fathers, and males did not avoid mating with their sisters, thus supporting inbreeding tolerance. Our experiments therefore add empirical evidence for inbreeding preference, which strengthens the prediction that inbreeding tolerance and preference can evolve under specific circumstances through the positive effects on inclusive fitness.     

On the evolution of polygyny: a theoretical examination of the polygyny threshold model

The polygyny threshold model states that if costs incurred areless than the benefits gained from mating polygynously in termsof breeding-situation quality, then polygyny is favored andcould evolve. We constructed mathematical models and computersimulations to evaluate this hypothesis. In the basic model,there is a single locus with two alleles, which regulates whetherthe female is receptive to polygyny. There are two breedingsituations of differing quality on which males randomly assort.Females then select a mate based on the associated breedingsituation and whether the male already has mates. This basicmodel is extended mathematically to include a cost for the initialfemale of a male with multiple mates and again to include geneexpression in males. The computer simulations extend the basicmodel to multiple loci and alleles and to multiple breedingsituations. The results presented here suggest that the polygynythreshold model is valid in a population genetic context: ifthe fitness of females that actually mate polygynously is greaterthan the fitness of monogamous females on poorer breeding situations,polygyny evolves. However, this approach reveals interestingdynamics not apparent from the verbal model. If the trait isexpressed in males and females, then polygyny can evolve evenif females mating polygynously have a lower fitness than femalesmating monogamously. In the multiple breeding-situations model,the polygyny allele increases to some equilibrium value abovewhich it experiences no selection. Surprisingly, as the costof polygyny increases, the equilibrium frequency of the polygynyallele also increases. The difference between this evolutionarymodel and the ideal free distribution is discussed.     

Reproduction of the Indian Meal Moth (Plodia interpunctella,lepidoptera, pyralidae): Mating success,polygyny, polyandry

The mating success of Plodia interpunctella was studied under the artificial conditions of polygyny and monoandry. More than 40% of the fecund females were fertilized without the actual transfer of a spermatophore. About 45% of the females did not lay eggs. Cases of complete sterility or low fertility of the females were recorded even in the cases when the spermatophore was transferred. On the whole, 70% of the matings were unsuccessful under the experimental conditions. It is suggested that incompatibility of mates is a very important factor in reproduction of P. interpunctella which increases the significance of polyandry and polygyny as mechanisms of increasing the number of males participating in reproduction.