Evolution Of Mating Preferences Research Articles

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.

Reinforcement of mate preference among hybridizingHeliconiusbutterflies

Recent models of mate preference evolution suggest that direct selection on alleles at preference loci and correlated evolution of preference with locally adapted mating cues are more likely to drive the evolution of assortative mate preference than reinforcement. Mate preference evolution in mimetic Heliconius butterflies has been attributed to all three forms of selection, but here we show that reinforcement has been critical. By examining geographical variation in assortative mating and male mate preference among seven populations of three hybridizing Heliconius species from Costa Rica, we found pronounced character displacement of preference such that sexual isolation was enhanced in areas of interspecific contact. Of the different explanations for the evolution of assortative mate preference, only reinforcement is dependent on interspecific contact in this system. Thus, the observed pattern of reproductive character displacement of mate preference is best explained as a product of indirect selection generated by natural selection against nonmimetic hybrids.

Sexual selection and mate choice

The past two decades have seen extensive growth of sexual selection research. Theoretical and empirical work has clarified many components of pre- and postcopulatory sexual selection, such as aggressive competition, mate choice, sperm utilization and sexual conflict. Genetic mechanisms of mate choice evolution have been less amenable to empirical testing, but molecular genetic analyses can now be used for incisive experimentation. Here, we highlight some of the currently debated areas in pre- and postcopulatory sexual selection. We identify where new techniques can help estimate the relative roles of the various selection mechanisms that might work together in the evolution of mating preferences and attractive traits, and in sperm-egg interactions.

Location, location, location: stripe position effects on female sword preference

The evolution of complex signals via sexual selection is becoming a primary focus in mate choice studies. Male swordtail fish, Xiphophorus helleri, have a secondary sexual trait, the sword, which is a composite trait consisting of four components favoured by sexual selection via female mate choice. The components include three coloured stripes and size. Although a complete sword is most attractive to female green swordtails, females prefer partial swords containing complete black stripes to incomplete swords lacking black coloration. Female swordtails also prefer longer swords. We addressed how subcomponents of the sword affect female mate choice. Digitally altered videos were used to investigate whether females respond differently to swords with proximal black stripes than to swords with distal black stripes. Although females preferred complete swords to both of the stimuli with partial stripes, they preferred males with distally striped swords to males with proximally striped swords. These results are discussed in light of hypotheses concerning the evolution of mating preferences for multicomponent traits. This study contributes to the growing body of information regarding the response of females to multicomponent visual traits.

Sensory Bias as an Explanation for the Evolution of Mate Preferences

The sensory bias model of sexual selection posits that female mating preferences are by-products of natural selection on sensory systems. Although sensory bias was proposed 20 years ago, its critical assumptions remain untested. This paradox arises because sensory bias has been used to explain two different phenomena. First, it has been used as a hypothesis about signal design, that is, that males evolve traits that stimulate female sensory systems. Second, sensory bias has been used as a hypothesis for the evolution of female preference itself, that is, to explain why females exhibit particular preferences. We focus on this second facet. First, we clarify the unique features of sensory bias relative to the alternative models by considering each in the same quantitative genetic framework. The key assumptions of sensory bias are that natural selection is the predominant evolutionary mechanism that affects preference and that sexual selection on preferences is quantitatively negligible. We describe four studies that would test these assumptions and review what we can and cannot infer about sensory bias from existing studies. We suggest that the importance of sensory bias as an explanation for the evolution of female preferences remains to be determined.

Variation between and within the sexes in body size preferences

Although it is often assumed that males and females have mating preferences for larger individuals of the other sex, potential underlying differences between male and female preferences for body size are not commonly investigated. Here, sexual differences in body size preferences are examined in the poeciliid fish, Brachyrhaphis rhabdophora. Females preferred larger males to smaller males, but preference did not appear to be affected by female size. One population-level analysis for males did not indicate an overall preference for larger females. A closer examination, however, revealed an effect of male size on preference; larger males preferred larger females, while smaller males preferred smaller females. It appears then that females, regardless of size, share a preference for large males, but males differ in their behaviour, depending on their body size. In addition, while the degree of difference in size between paired females did not appear to affect male preference, the degree of difference in size between paired males strongly affected female preference; the greater the difference, the more strongly females preferred the larger male. Thus, intersexual selection is found to operate in both sexes, but how it operates appears to differ. Intrasexual and intersexual differences in mating behaviour may be missed when evaluating population-wide preferences. That is, there can be underlying differences in how the sexes respond and the consequences of such differences should be considered when investigating mate choice. The results are considered in terms of the evolution of mating preferences, alternative mating strategies, assortative mating, the maintenance of trait variation in a population, and current methods to evaluate mating preferences.

Variation between and within the sexes in body size preferences

Although it is often assumed that males and females have mating preferences for larger individuals of the other sex, potential underlying differences between male and female preferences for body size are not commonly investigated. Here, sexual differences in body size preferences are examined in the poeciliid fish, Brachyrhaphis rhabdophora . Females preferred larger males to smaller males, but preference did not appear to be affected by female size. One population-level analysis for males did not indicate an overall preference for larger females. A closer examination, however, revealed an effect of male size on preference; larger males preferred larger females, while smaller males preferred smaller females. It appears then that females, regardless of size, share a preference for large males, but males differ in their behaviour, depending on their body size. In addition, while the degree of difference in size between paired females did not appear to affect male preference, the degree of difference in size between paired males strongly affected female preference; the greater the difference, the more strongly females preferred the larger male. Thus, intersexual selection is found to operate in both sexes, but how it operates appears to differ. Intrasexual and intersexual differences in mating behaviour may be missed when evaluating population-wide preferences. That is, there can be underlying differences in how the sexes respond and the consequences of such differences should be considered when investigating mate choice. The results are considered in terms of the evolution of mating preferences, alternative mating strategies, assortative mating, the maintenance of trait variation in a population, and current methods to evaluate mating preferences.

A possible non-sexual origin of mate preference: are male guppies mimicking fruit?

In most animals, the origins of mating preferences are not clear. The "sensory-bias" hypothesis proposes that biases in female sensory or neural systems are important in triggering sexual selection and in determining which male traits will become elaborated into sexual ornaments. Subsequently, other mechanisms can evolve for discriminating between high- and low-quality mates. Female guppies (Poecilia reticulata) generally show a preference for males with larger, more chromatic orange spots. It has been proposed that this preference originated because it enabled females to obtain high-quality mates. We present evidence for an alternative hypothesis, that the origin of the preference is a pleiotropic effect of a sensory bias for the colour orange, which might have arisen in the context of food detection. In field and laboratory experiments, adult guppies of both sexes were more responsive to orange-coloured objects than to objects of other colours, even outside a mating context. Across populations, variation in attraction to orange objects explained 94% of the inter-population variation in female mate preference for orange coloration on males. This is one of the first studies to show both an association between a potential trigger of a mate-choice preference and a sexually selected trait, and also that an innate attraction to a coloured inanimate object explains almost all of the observed variation in female mate choice. These results support the "sensory-bias" hypothesis for the evolution of mating preferences.

Carotenoid limitation and mate preference evolution: a test of the indicator hypothesis in guppies (Poecilia reticulata).

Under the indicator models of mate choice, female preferences evolve to exploit the condition-dependence or "indicator value" of male traits, which in turn may cause these traits to evolve to elaborate extremes. If the indicator value of a male trait changes, the payoff function of the female preference for that trait should change and the preference should evolve to a new optimum. I tested this prediction in the guppy, Poecilia reticulata, a species in which the indicator value of a sexually selected male trait, carotenoid coloration, varies geographically. Carotenoid coloration is thought to be an indicator of foraging ability and health because animals must obtain carotenoid pigments from their diet. The primary dietary source of carotenoids for guppies is unicellular algae, the abundance of which varies among natural streams because of variation in forest canopy cover. Carotenoid availability limits male coloration to a greater extent in streams with greater forest canopy cover. Thus, the indicator value of male coloration covaries positively with canopy cover. To test the indicator model prediction, I measured genetic divergence in the strength of female preferences for carotenoid coloration between high- and low-carotenoid availability streams in each of three river drainages. Second-generation laboratory-born females were given a choice between full-sib males raised on three different dietary levels of carotenoids. For all six populations, male attractiveness (as determined from the responses of females to male courtship displays) increased with dietary carotenoid levels. However, the strength of female preferences differed between populations in the predicted direction in only one of three river drainages. These results fail to support a crucial prediction of the indicator model. More studies taking an interpopulation approach to studying mate preference evolution are needed before the explanatory value of the indicator models can be rigorously assessed.

The evolution of sex.

Birds do it, bees do it, people do it—in fact the vast majority of organisms do it—but sexual reproduction often seems more trouble than it's worth. For organisms, sex often means spending huge amounts of energy finding and wooing desirable partners. Within the cell, male and female genomes must recombine without major mistakes. Gametes must promote compatible fusions while upholding barriers between species. And at each step, the conflicting interests of each sex must be delicately negotiated in order to benefit the species as a whole. Asexual reproduction—a simple “copy and divide” strategy—at first glance seems both less messy and more efficient. Yet sexual reproduction is by far the dominant mode, which leads researchers to conclude that sex offers some evolutionary advantage. Biologists have been spinning theories about just what that advantage might be for quite some time, but so far there is no single clear answer. The debate continues energetically, however, as shown in the news stories and review articles in this special section on the evolution of sex. The topic falls into two parts. First, why did sex evolve in the first place and why is it so pervasive in the natural world? And secondly, how do these amazingly complex sexual systems evolve? The News story by [Wuethrich][1] and article by [Barton and Charlesworth][2] address the first of these questions—what makes sex so alluring from an evolutionary standpoint? Barton and Charlesworth conclude that genetic recombination seems to be the key. Indeed, as discussed in both pieces, most theories suggest that sex and recombination remove harmful mutations and allow new combinations of genes to come together, providing more opportunities for improved fitness and offering the flexibility to adapt to new environments. Biologists are finding new ways to test these theories, Wuethrich reports, but proving that they are actually operating in the natural world remains a challenge. Once sexual reproduction is in place, what cellular and behavioral mechanisms build the system? In their article, [Marin and Baker][3] discuss the evolution of genes that dictate the differential development of the sexes. Some of these genes are stable in evolutionary terms while others, particularly the regulatory genes at the top of the developmental cascade, are changing rapidly. The process by which sperm and egg recognize compatible cognates also involves unusually rapid evolution, as discussed in [Vacquier's article][4]. The greatest variety seems to be found in the diverse chemoattractants and surface receptors that promote fusion between the right pair of gametes. As any human knows, complex mating rituals are often a critical part of reproduction. [Ryan's article][5] explores the evolution of mating preferences and discusses the effects of receiver bias—or, how beauty is in the eye of the beholder. Both historical effects and expressed female preferences affect the evolution of characteristically male traits. Although the sexes come together to mate, their evolutionary interests often conflict. [Partridge and Hurst's article][6] provides an overview of the often opposing forces driving the evolution of female and male and the molecular expressions of the war between the sexes. Two News stories explore particular manifestations of this conflict. [Morell][7] takes a new look at monogamy, the one mating system where conflict would seem to be at a minimum. Yet recent research has shown that in many species, females once thought to be monogamous bear offspring with different fathers. Even when social bonds are strong, extrapair matings apparently offer evolutionary advantage. And [Pennisi][8] reports on one genetic weapon wielded in the battle of the sexes: genomic imprinting, in which genes from one parent are marked for later silencing or disposal. Mammalian researchers argue that imprinting represents a battle over the growth rate of the fetus, and have new data to bolster their case. Thus, a growing body of research demonstrates that in interactions ranging from molecular to social, sexual reproduction thrives in a metastable state, balancing conflict and resolution—and remaining the most effective reproductive strategy available. [1]: /lookup/doi/10.1126/science.281.5385.1980 [2]: /lookup/doi/10.1126/science.281.5385.1986 [3]: /lookup/doi/10.1126/science.281.5385.1990 [4]: /lookup/doi/10.1126/science.281.5385.1995 [5]: /lookup/doi/10.1126/science.281.5385.1999 [6]: /lookup/doi/10.1126/science.281.5385.2003 [7]: /lookup/doi/10.1126/science.281.5385.1982 [8]: /lookup/doi/10.1126/science.281.5385.1984

The evolution of mate choice and the potential for conflict between species and mate–quality recognition

Understanding how individuals select mates becomes complex when high-quality conspecifics resemble heterospecifics. Individuals facing such a situation may be unable to effectively identify both conspecifics (species recognition) and high-quality mates that can confer fitness benefits to the choosy individual or its offspring (mate-quality recognition). Here I suggest when a conflict may occur between species and mate-quality recognition, discuss the evolutionary consequences stemming from this conflict, and present a model of mate-preference evolution in response to heterospecifics. Determining how species and mate-quality recognition interact to shape mate-choice decisions is important for understanding the diversification of sexually selected traits among closely related taxonomic groups, the use of complex sensory systems for detecting mates, and seemingly inappropriate mate-choice decisions.

The Evolution Of Indicator Traits For Parental Quality: The Role Of Maternal And Paternal Effects

In systems where individuals provide material resources to their mates or offspring, mate choice based on traits that are phenotypically correlated with the quality of resources provided is expected to be adaptive. Several models have explored the evolution of mating preference where there are direct benefits to choice, but few have addressed how a phenotypic correlation can be established between a male indicator trait and the degree of parental investment. We present a model with three quantitative traits: male and female parental investment and a potential male indicator trait. In our model, the expression of the "indicator" trait in offspring is affected by parental investment. These effects are referred to as maternal or paternal effects, or as "indirect genetic effects" when parental investment is heritable. With genetic variation for degree of parental investment, offspring harbor genes for parental investment that are unexpressed before mating but will affect the investment that they provide when expressed. Because the investment received from the parents affects the expression of the indicator trait, there will be a correlation between the genes for parental investment inherited and the degree of expression of the indicator trait in the offspring. The indicator trait is thus an "honest" signal for the degree of paternal investment.

The Phylogenetic Distribution of a Female Preference

Robust phylogenetic information can be instrumental to the study of the evolution of female mating preferences and preferred male traits. In this paper, the evolution of a preexisting female bias favoring a sword in male swordtail fish and the evolution of the sword, a complex character, are used to demonstrate how the evolution of mating preferences and preferred traits can be examined in a phylogenetic context. Phylogenetic information suggests that a preference for a sword arose prior to the evolution of the sword in the genus Xiphophorus and that the sword was adaptive at its origin. A phylogenetic approach to the study of female preferences and male traits can also be informative when used in conjunction with mate choice theory in making predictions about evolutionary changes in an initial bias, both prior to the appearance of the male trait it favors and subsequent to the appearance of the trait. (Mate choice; female preference; preexisting biases; Priapella; swordtail; sword; Xiphophorus.) The study of the evolution of mating preferences is an area of much contention. Until relatively recently, there was dis- agreement over the importance of female mate choice. In the past 15 years, however, many studies have shown that females ex- hibit mating preferences and that these mating preferences can have an important

The Evolution of Mate Preferences for Multiple Sexual Ornaments

The Evolution of Mate Preferences for Multiple Sexual Ornaments

The evolution of mating preferences and the paradox of the lek

Why do females prefer elaborate male mating displays in species where they receive little more from males than their sperm? Here we review three hypotheses for the evolution of mating preferences: direct selection, the runaway process and the parasite mechanism. There is growing support for direct selection, in which preferences evolve because of their direct effects on female fitness rather than the genetic effects on offspring resulting from mate choice.

The role of amplifiers in sexual selection: An integration of the amplifying and the Fisherian mechanisms

In a non-Fisherian genetic model I have shown that sexual displays can evolve even if displays are not directly and unconditionally preferred by females (a basic requirement in any Fisherian model), provided that they amplify previously recognized differences in male quality. Here I show how this amplifying mechanism interacts with the traditional Fisherian mechanism of sexual selection. The theory that integrates these two mechanisms provides a more robust, entirely selective scenario of the evolution of mating preferences and sexual displays.

THE DARWIN-FISHER THEORY OF SEXUAL SELECTION IN MONOGAMOUS BIRDS.

Males of monogamous birds often show secondary sexual traits that are conspicuous but considerably less extreme than those of polygynous species. We develop a quantitative-genetic model for the joint evolution of a male secondary sexual trait, a female mating preference, and female breeding date, following a theory proposed by Darwin and Fisher. Good nutritional condition is postulated to cause females to breed early and to have high fecundity. The most-preferred males are mated by early-breeding females and receive a sexual-selection advantage from those females' greater reproductive success. Results show that conspicuous male traits that decrease survival can evolve but suggest that the extent of maladaptive evolution is greatly limited relative to what is possible in a polygynous mating system for two reasons. First, in the absence of direct fitness effects of mate choice on the female, the equilibria for the male trait and female preference form a curve whose shape shows that the maximum possible strength of sexual selection on males (and hence the potential for maladaptive evolution) is constrained. Under certain conditions, a segment of the equilibrium curve may become unstable, leading to two alternative stable states for the male trait. Second, male parental care will often favor the evolution of mating preferences for less conspicuous males. We also find that sexual selection can appear in the absence of the nutritional effects emphasized by Darwin and Fisher. A review of the literature suggests that the assumptions of the Darwin-Fisher mechanism may often be met in monogamous birds and that other mechanisms may often reinforce it by producing additional components of sexual selection.

Fisherian and Wrightian theories of speciation.

Fisher's theory of sexual selection, Wright's shifting-balance theory, and recent models based on them are reviewed as mechanisms of animal speciation. The joint evolution of mating preferences and secondary sexual characters can cause rapid nonadaptive phenotypic divergence and premating isolation between geographically separated populations, or along a cline. Extensive comparative data on Drosophila species support the suggestion of R. A. Fisher and T. Dobzhansky that the evolution of mating preferences can reinforce partial postmating isolation between sympatric populations. The interaction of natural selection and random genetic drift in local populations with a small effective size can produce a rapid transition between relatively stable phenotypes separated by an adaptive valley, or between chromosomal rearrangements with a heterozygote disadvantage. Large demographic fluctuations, such as frequent random local extinction and colonization, are required for the rapid spread of new adaptations (or karyotypes) when intermediate phenotypes (or rearrangement heterozygotes) are selected against.

Condition-Dependent Sex Ornaments and Field Tests of Sexual-Selection Theory

Condition-Dependent Sex Ornaments and Field Tests of Sexual-Selection Theory