Evolution Of Mating Preferences Research Articles

The evolution of mating preferences for genetic attractiveness and quality in the presence of sensory bias

The aesthetic preferences of potential mates have driven the evolution of a baffling diversity of elaborate ornaments. Which fitness benefit-if any-choosers gain from expressing such preferences is controversial, however. Here, we simulate the evolution of preferences for multiple ornament types (e.g., "Fisherian," "handicap," and "indicator" ornaments) that differ in their associations with genes for attractiveness and other components of fitness. We model the costs of preference expression in a biologically plausible way, which decouples costly mate search from cost-free preferences. Ornaments of all types evolved in our model, but their occurrence was far from random. Females typically preferred ornaments that carried information about a male's quality, defined here as his ability to acquire and metabolize resources. Highly salient ornaments, which key into preexisting perceptual biases, were also more likely to evolve. When males expressed quality-dependent ornaments, females invested readily in costly mate search to locate preferred males. In contrast, the genetic benefits associated with purely arbitrary ornaments were insufficient to sustain highly costly mate search. Arbitrary ornaments could nonetheless "piggyback" on mate-search effort favored by other, quality-dependent ornaments. We further show that the potential to produce attractive male offspring ("sexy sons") can be as important as producing offspring of high general quality ("good genes") in shaping female preferences, even when preferred ornaments are quality dependent. Our model highlights the importance of mate-search effort as a driver of aesthetic coevolution.

From Material to Non-Material Needs? The Evolution of Mate Preferences through the Twentieth Century in France

This paper studies the evolution of mate preferences throughout the twentieth century in France. I digitized all the matrimonial ads published in France’s best-selling monthly magazine from 1928 to 1994. Using dictionary-based methods, I show that mate preferences were mostly stable during the Great Depression, WWII, and the ensuing economic boom. These preferences started transforming in the late 1960s when economic criteria were progressively replaced by personality criteria. The timing coincides with profound family and demographic changes in French society. These findings suggest that, in the search for a long-term partner, non-material needs have replaced material ones.

Visual mate preference evolution during butterfly speciation is linked to neural processing genes

Many animal species remain separate not because their individuals fail to produce viable hybrids but because they “choose” not to mate. However, we still know very little of the genetic mechanisms underlying changes in these mate preference behaviours. Heliconius butterflies display bright warning patterns, which they also use to recognize conspecifics. Here, we couple QTL for divergence in visual preference behaviours with population genomic and gene expression analyses of neural tissue (central brain, optic lobes and ommatidia) across development in two sympatric Heliconius species. Within a region containing 200 genes, we identify five genes that are strongly associated with divergent visual preferences. Three of these have previously been implicated in key components of neural signalling (specifically an ionotropic glutamate receptor and two regucalcins), and overall our candidates suggest shifts in behaviour involve changes in visual integration or processing. This would allow preference evolution without altering perception of the wider environment.

Reviewing guppy color vision: integrating the molecular and physiological variation in visual tuning of a classic system for sensory drive.

Sensory drive predicts coevolution of mate choice signals with the sensory systems detecting those signals. Guppies are a classic model for sensory drive as mate preferences based on coloration differ across individuals and populations. A large body of work has identified variation in color vision, yet we lack a direct tie between how such variation in color vision influences variation in color preference. Here we bring together studies that have investigated guppy vision over the past 40 years to: (1) highlight our current understanding of where variation occurs in the guppy color vision pathway and (2) suggest future avenues of research into sources of visual system variation that could influence guppy color preference. This will allow researchers to design careful studies that couple measures of color preference with measures of visual system variation from the same individual or population. Such studies will finally provide important answers as to what sets the direction and speed of mate preference evolution via sensory drive.

Spatial and temporal variation in three call traits and preferences of the tree cricket Oecanthus forbesi

Multiple selective forces act on the evolution of mating preferences. While mating preferences are central to pre-zygotic isolation, certain preferences and traits may make greater contributions. For some traits, females may exhibit preferences, but accept heterospecifics trait values when preferred values are scarce. For other traits, females may fail to reproduce before accepting heterospecifics trait values. Understanding patterns of variation and divergence in this later class of traits is particularly relevant to understanding divergence and speciation. Here, I focus on three call traits of Forbes’ Tree Cricket (Oecanthus forbesi) to quantify their capacity to produce reproductive isolation and to compare patterns of variation and divergence in these traits. By generating female preference functions and measuring male call parameters, I test two hypotheses: (1) traits and preferences vary in their capacity to contribute to reproductive isolation and (2) traits that are important to reproductive isolation have lower intrapopulation, interpopulation, and interannual variation and weaker correlation with male body size. I find that female response to one trait (pulse rate) decreased sharply when trait values fell within the heterospecific range. This trait had low variation and no correlation with male morphology. For two other traits (pulse duration and dominant frequency), females responded to many values, including values characteristics of co-occurring heterospecifics. Trait variation was higher and pulse duration correlated with male leg length. These results indicate that the evolutionary dynamics of a low-variation trait (pulse rate) may be more important to speciation than changes in more conspicuously variable sexually selected traits. Animals often attract and assess mates using complex signals. This paper tests whether some signal components contribute more to preventing mating between species. The data show that changes in a single trait [pulse rate of cricket calls] can eliminate female response to males, while other traits [dominant frequency (pitch) and pulse duration] can be changed to match the values produced by other species without reducing female response. Consequently, some traits may diverge without contributing to reproductive isolation between species. The paper then tests for correlations between trait function and patterns of trait variation within and between populations and species. Pulse rate has low variation within and between populations, but differs substantially between species. Dominant frequency and pulse rate are more variable within and between populations. Pulse duration also correlates with male body size, indicating that pulse duration could reflect male condition even if it is relatively unimportant for reproductive isolation.

What is driving male mate preference evolution in Jamaican field crickets?

ABSTRACTMale mating preferences are often a neglected aspect of studies on sexual selection. Male mating preferences may evolve if they provide males with direct‐fitness benefits such as increased opportunity to fertilize more eggs or indirect‐fitness benefits such as enhanced offspring survival. We tested these ideas using Jamaican field crickets, Gryllus assimilis, previously shown to exhibit male mating preferences. We randomly mated males to either their preferred or non‐preferred potential mates and then asked whether mating treatment influenced egg oviposition or offspring viability. Preferred females were not significantly more fecund and did not produce more viable eggs or offspring than non‐preferred females. Male mate preferences were therefore inconsistent with both the direct‐ and indirect‐fitness benefits hypotheses under the conditions of our experiment. Our null results leave us with an open question about what is driving the evolution of mating preferences in male crickets. Future research should explore the whether the offspring of preferred females are more attractive, have stronger immune systems, and/or experience higher adult longevity.

Aesthetic evolution by mate choice: Darwin'sreallydangerous idea

Darwin proposed an explicitly aesthetic theory of sexual selection in which he described mate preferences as a 'taste for the beautiful', an 'aesthetic capacity', etc. These statements were not merely colourful Victorian mannerisms, but explicit expressions of Darwin's hypothesis that mate preferences can evolve for arbitrarily attractive traits that do not provide any additional benefits to mate choice. In his critique of Darwin, A. R. Wallace proposed an entirely modern mechanism of mate preference evolution through the correlation of display traits with male vigour or viability, but he called this mechanism natural selection. Wallace's honest advertisement proposal was stridently anti-Darwinian and anti-aesthetic. Most modern sexual selection research relies on essentially the same Neo-Wallacean theory renamed as sexual selection. I define the process of aesthetic evolution as the evolution of a communication signal through sensory/cognitive evaluation, which is most elaborated through coevolution of the signal and its evaluation. Sensory evaluation includes the possibility that display traits do not encode information that is being assessed, but are merely preferred. A genuinely Darwinian, aesthetic theory of sexual selection requires the incorporation of the Lande-Kirkpatrick null model into sexual selection research, but also encompasses the possibility of sensory bias, good genes and direct benefits mechanisms.

Context-dependent male mate choice: the effects of competitor presence and competitor size

Differences in the intensity of male–male competition for high- and low-quality females affect their value as mates. This can favor the evolution of mating preferences that vary with inherent male competitiveness and/or context-dependent mate choice. In the eastern mosquitofish (Gambusia holbrooki) we investigated how a male’s choice of mate is influenced by his absolute size when alone (baseline mating preference) and by the presence and relative size of a competitor (context dependent). In standard 2choice mating trials, we compared the time in association with the larger of 2 females in: 1) the absence of a rival; 2) the presence of a same-sized rival, and 3) the presence of a different-sized rival. We predicted which female the focal male would choose based on his estimated reproductive success. In all 3 social contexts, large and small focal males spent significantly more time with large females, but large males had a stronger association bias, indicating an effect of male size (competitiveness) on male mating preference. In contrast, neither the presence of a competitor nor his relative size affected the time the focal male spent with the large female. There was therefore no evidence that males facultatively adjust mate choice decisions to avoid competitors. This suggests that males do not maximize their expected reproductive success in the context of the current social setting. Key words: eastern mosquitofish, Gambusia holbrooki, male–male competition, mating preferences, sexual selection. [Behav Ecol]

The Evolution of Sex-Related Traits and Genes

The Evolution of Sex-Related Traits and Genes

Does sexual selection evolve following introduction to new environments?

The rate of evolution of mating preferences and mate signalling traits can influence local adaptation and diversification under environmental change. However, the rate of evolution of female preferences has not been directly examined in natural populations. An opportunity to do so arose through the introduction of high-predation Trinidadian guppies, Poecilia reticulata, from the Yarra River into high- and low-predation environments in the Damier River. Nine years (13–26 guppy generations) after the introduction, we tested whether female preferences for key aspects of male colour differed between the rivers and between introduced high- and low-predation populations. Based on two independent laboratory experiments, we conclude that little divergence in female preferences has apparently occurred between any of the populations, or between predation regimes. In combination with previous work, these results suggest that the evolution of guppy colour and female preferences are influenced by factors in addition to just predation, and that female preferences may generally take longer to evolve than other types of traits, particularly in populations that experience weak or fluctuating sexual selection gradients.

A review and perspective on context-dependent genetic effects of extra-pair mating in birds

The evolutionary origin and the maintenance of extra-pair mating in birds has been a major field of study in the last decades, but no consensus has been reached on the adaptive significance of this behaviour for female birds. The genetic benefit hypothesis proposes that extra-pair sires provide alleles of superior quality and/or better compatibility compared to the social mate, resulting in offspring of higher reproductive value. One frequently adopted approach to test this idea compares the performance of maternal half-siblings in broods with multiple paternity. However, results from such comparisons are inconsistent. Here I discuss the concept that the magnitude of genetic fitness benefits from extra-pair mating depends on the environmental context. To date, context-dependent genetic effects in maternal half-sibling comparisons have been demonstrated for only five passerine bird species. In none of the studies were the crucial environmental conditions experimentally manipulated, and the potentially confounding effects of differential maternal investment in relation to paternity were also largely not accounted for. A number of high-quality data sets on fitness consequences of extra-pair mating behaviour are available that could be (re-) analysed for context-dependence given that relevant gradients of the environment have been recorded and their use is well justified a priori. Such relevant variation may include, for example, the time of breeding in temperate regions, hatching order, but also offspring sex. Primarily, however, experimental approaches are required that systematically and gradually vary fitness-relevant environmental gradients, such as food availability or parasite abundance, and analyse the resulting differential fitness effects while controlling for differential investment. The context dependency of the genetic effects of extra-pair mating behaviour may offer an opportunity for reconciling conflicting results from different extra-pair paternity studies within and across species. More generally, it could allow a better understanding of under which environmental conditions will selection act to maintain a female mating bias towards extra-pair males with potentially far-reaching implications for the ecology and evolution of mating preferences and the maintenance of genetic variation in (sexually) selected traits.

Me, myself and I

Flowering plants have diversified and conquered the land. To do so, they have evolved strategies to avoid incest and promote compatible outcrossing. Philip Hunter explores some of the latest research in this area and its application to agriculture and horticulture.

On the Origin of Species by Natural and Sexual Selection

Ecological speciation is considered an adaptive response to selection for local adaptation. However, besides suitable ecological conditions, the process requires assortative mating to protect the nascent species from homogenization by gene flow. By means of a simple model, we demonstrate that disruptive ecological selection favors the evolution of sexual preferences for ornaments that signal local adaptation. Such preferences induce assortative mating with respect to ecological characters and enhance the strength of disruptive selection. Natural and sexual selection thus work in concert to achieve local adaptation and reproductive isolation, even in the presence of substantial gene flow. The resulting speciation process ensues without the divergence of mating preferences, avoiding problems that have plagued previous models of speciation by sexual selection.

Heterozygosity-based assortative mating in blue tits (Cyanistes caeruleus): implications for the evolution of mate choice

The general hypothesis of mate choice based on non-additive genetic traits suggests that individuals would gain important benefits by choosing genetically dissimilar mates (compatible mate hypothesis) and/or more heterozygous mates (heterozygous mate hypothesis). In this study, we test these hypotheses in a socially monogamous bird, the blue tit (Cyanistes caeruleus). We found no evidence for a relatedness-based mating pattern, but heterozygosity was positively correlated between social mates, suggesting that blue tits may base their mating preferences on partner's heterozygosity. We found evidence that the observed heterozygosity-based assortative mating could be maintained by both direct and indirect benefits. Heterozygosity reflected individual quality in both sexes: egg production and quality increased with female heterozygosity while more heterozygous males showed higher feeding rates during the brood-rearing period. Further, estimated offspring heterozygosity correlated with both paternal and maternal heterozygosity, suggesting that mating with heterozygous individuals can increase offspring genetic quality. Finally, plumage crown coloration was associated with male heterozygosity, and this could explain unanimous mate preferences for highly heterozygous and more ornamented individuals. Overall, this study suggests that non-additive genetic traits may play an important role in the evolution of mating preferences and offers empirical support to the resolution of the lek paradox from the perspective of the heterozygous mate hypothesis.

Divergent female mating preference in a clonal fish

In asexual all-female species, such as the Amazon molly, Poecilia formosa, that depend on sperm from “host males” only to trigger embryogenesis, mate choice does not provide any indirect, genetic benefits to the choosing female, although direct benefits are possible. Asexual species are thought to have a low evolutionary potential or evolvability due to the absence of meiotic recombination. Hence, theory predicts that mating preferences in P. formosa for male ornaments—if existent—should resemble those of females of the two parental species (Poecilia latipinna and Poecilia mexicana) involved in the natural hybridization that gave rise to the asexual P. formosa. When examining the female preference for dummy males with or without black vertical bars in the two parental species and in two lineages of P. formosa, a preference was detected in P. latipinna, but not in P. mexicana females. Interestingly, P. formosa living syntopic with P. latipinna also preferred striped males, while others living syntopic with P. mexicana preferred non-striped males. The evolutionary significance of this phenomenon remains largely unexplained, but it might indicate the evolution of mating preferences in a species with low evolutionary potential. Possible mechanisms include introgression and mitotic gene conversion. Females might use male coloration as indicator mechanisms for male traits that matter in terms of direct benefits.

A TEST OF THE CRITICAL ASSUMPTION OF THE SENSORY BIAS MODEL FOR THE EVOLUTION OF FEMALE MATING PREFERENCE USING NEURAL NETWORKS

The sensory bias model for the evolution of mating preferences states that mating preferences evolve as correlated responses to selection on nonmating behaviors sharing a common sensory system. The critical assumption is that pleiotropy creates genetic correlations that affect the response to selection. I simulated selection on populations of neural networks to test this. First, I selected for various combinations of foraging and mating preferences. Sensory bias predicts that populations with preferences for like-colored objects (red food and red mates) should evolve more readily than preferences for differently colored objects (red food and blue mates). Here, I found no evidence for sensory bias. The responses to selection on foraging and mating preferences were independent of one another. Second, I selected on foraging preferences alone and asked whether there were correlated responses for increased mating preferences for like-colored mates. Here, I found modest evidence for sensory bias. Selection for a particular foraging preference resulted in increased mating preference for similarly colored mates. However, the correlated responses were small and inconsistent. Selection on foraging preferences alone may affect initial levels of mating preferences, but these correlations did not constrain the joint evolution of foraging and mating preferences in these simulations.

Gentlemen Prefer Blondes: The Evolution of Mate Preference among Strategically Allocated Males

Male mate selection during polygyny traditionally has been eclipsed in the literature by its female counterpart. Existing models that have studied male mate choice have concluded that males with genetically inherited preferences for females exhibiting particular traits are often less fit than males without such a preference, leading to preference loss. In this article, we explore the consequences of a fundamental difference between male and female mate choice, the way in which the opposite sex acts as a resource during mating. By incorporating a strategic process at the ecological level, we show that if males are allowed to actively adjust the distribution of their courtship efforts over the available classes of females, male preference can be maintained as a polymorphism. Further, the resulting coexistence induces a reproductive segregation within the population that, when coupled with genetic control of female traits, can lead to strong linkage disequilibrium between the alleles for trait and preference. These processes can cause complete assortative mating to emerge in the model.

Females prefer the scent of outbred males: good-genes-as-heterozygosity?

BackgroundThere is increasing interest to determine the relative importance of non-additive genetic benefits as opposed to additive ones for the evolution of mating preferences and maintenance of genetic variation in sexual ornaments. The 'good-genes-as-heterozygosity' hypothesis predicts that females should prefer to mate with more heterozygous males to gain more heterozygous (and less inbred) offspring. Heterozygosity increases males' sexual ornamentation, mating success and reproduction success, yet few experiments have tested whether females are preferentially attracted to heterozygous males, and none have tested whether females' own heterozygosity influences their preferences. Outbred females might have the luxury of being more choosey, but on the other hand, inbred females might have more to gain by mating with heterozygous males. We manipulated heterozygosity in wild-derived house mice (Mus musculus musculus) through inbreeding and tested whether the females are more attracted to the scent of outbred versus inbred males, and whether females' own inbreeding status affects their preferences. We also tested whether infecting both inbred and outbred males with Salmonella would magnify females' preferences for outbred males.ResultsFemales showed a significant preference for outbred males, and this preference was more pronounced among inbred females. We found no evidence that Salmonella infection increased the relative attractiveness of outbred versus inbred males; however, we found no evidence that inbreeding affected males' disease resistance in this study.ConclusionOur findings support the idea that females are more attracted to outbred males, and they suggest that such preferences may be stronger among inbred than outbred females, which is consistent with the 'good-genes-as-heterozygosity' hypothesis. It is unclear whether this odour preference reflects females' actual mating preferences, though it suggests that future studies should consider females' as well as males' heterozygosity. Our study has implications for efforts to understand how mate choice can provide genetic benefits without eroding genetic diversity (lek paradox), and also conservation efforts to determine the fitness consequences of inbreeding and the maintenance of genetic diversity in small, inbred populations.

INCIPIENT SEXUAL ISOLATION AMONG COSMOPOLITANDROSOPHILA MELANOGASTERPOPULATIONS

Understanding the biological conditions and the genetic basis of early stages of sexual isolation and speciation is an outstanding question in evolutionary biology. It is unclear how much genetic and phenotypic variation for mating preferences and their phenotypic cues is segregating within widespread and human-commensal species in nature. A recent case of incipient sexual isolation between Zimbabwe and cosmopolitan populations of the human-commensal fruit fly Drosophila melanogaster indicates that such species may initiate the process of sexual isolation. However, it is still unknown whether other geographical populations have undergone evolution of mating preferences. In this study we present new data on multiple-choice mating tests revealing partial sexual isolation between the United States and Caribbean populations. We relate our findings to African populations, showing that Caribbean flies are partially sexually isolated from Zimbabwe flies, but mate randomly with West African flies, which also show partial sexual isolation from the United States and Zimbabwe flies. Thus, Caribbean and West African populations seem to exhibit distinct mating preferences relative to populations in the United States and in Zimbabwe. These results suggest that widespread and human-commensal species may harbor different types of mating preferences across their geographical ranges.

Maternal effects of carotenoid consumption in guppies (Poecilia reticulata)

Summary 1. Carotenoids transferred from mother to offspring may enhance the quality of the offspring. Whether such maternal effects occur in guppies ( Poecilia reticulata ) has an important bearing on mate preference evolution. 2. By raising female guppies from birth on different dietary carotenoid levels, we examined the pattern of carotenoid allocation to maternal tissue (skin) vs. eggs. Skin carotenoid content was only weakly affected by carotenoid intake while egg carotenoid content was strongly affected. 3. We then tested for effects of maternal carotenoid intake on several measures of offspring quality, including size and condition at birth, juvenile growth rate, and the size, condition, skin carotenoid content and colouration of mature sons. To test for interactions between maternal and offspring carotenoid intake, broods were split and offspring were reared on one of two carotenoid levels. 4. Offspring carotenoid intake had the expected effects on male colouration, but otherwise we found no evidence that maternal or offspring carotenoid intake influences offspring quality. It remains possible that maternal carotenoids affect offspring fitness parameters that we did not measure or that such effects depend on environmental factors that were absent in our laboratory aquaria. 5. Our review of the literature on maternal carotenoid effects in birds and fishes suggests that such effects may be taxon-specific. Thus, it seems unwarranted to assume that an adaptive trade-off necessarily exists between allocation of carotenoids to eggs vs. maternal tissues. Alternative hypotheses, such as the possibility that eggs provide a means of excreting excess carotenoids, also merit consideration. 6. Our results indirectly support the indicator model of mate preference evolution by casting doubt on an alternative hypothesis that requires females to benefit more from consuming carotenoids than males do.