Why do ovigerous females approach courting males? Female preferences and sensory biases in a fiddler crab

Perceptual biases explain the origin and evolution of female preference in many species. Some responses that mediate mate choice, however, may have never been used in nonmating contexts. In the fiddler crab, Uca mjoebergi, mate‐searching females prefer faster wave rates and leading wave; however, it remains unclear whether such responses evolved in a mating context (i.e., the preference has effect on the fitness of the female and her offspring that arise from mating with a particular male) or a nonmating contexts (i.e., a female obtains direct benefits through selecting the male with a more detectable trait). Here, we compared the preferences of mate‐searching with those of ovigerous females that are searching for a burrow and do not concern about male “quality.” Results showed that as both mate‐searching and ovigerous females preferentially approached robotic males with faster wave rates. This suggests that wave rate increases detectability/locatability of males, but the mating preference for this trait is unlikely to evolve in the mating context (although it may currently function in mate choice), as it does not provide fitness‐related benefit to females or her offspring. Wave leadership, in contract, was attractive to mate‐searching females, but not ovigerous females, suggesting that female preference for leadership evolves because wave leadership conveys information about male quality. We provide not only an empirical evidence of sensory biases (in terms of the preference for faster wave), but the first experimental evidence that mating context can be the only selection force that mediates the evolution of male sexual traits and female preference (in terms of the preference for leading wave).     

Sexual selection and assortative mating: an experimental test

Mate choice and mate competition can both influence the evolution of sexual isolation between populations. Assortative mating may arise if traits and preferences diverge in step, and, alternatively, mate competition may counteract mating preferences and decrease assortative mating. Here, we examine potential assortative mating between populations of Drosophila pseudoobscura that have experimentally evolved under either increased (‘polyandry’) or decreased (‘monogamy’) sexual selection intensity for 100 generations. These populations have evolved differences in numerous traits, including a male signal and female preference traits. We use a two males: one female design, allowing both mate choice and competition to influence mating outcomes, to test for assortative mating between our populations. Mating latency shows subtle effects of male and female interactions, with females from the monogamous populations appearing reluctant to mate with males from the polyandrous populations. However, males from the polyandrous populations have a significantly higher probability of mating regardless of the female's population. Our results suggest that if populations differ in the intensity of sexual selection, effects on mate competition may overcome mate choice.     

The evolution of phenotypes and genetic parameters under preferential mating

This article extends and adds more realism to Lande's analytical model for evolution under mate choice by using individual‐based simulations in which females sample a finite number of males and the genetic architecture of the preference and preferred trait evolves. The simulations show that the equilibrium heritabilities of the preference and preferred trait and the genetic correlation between them (r_G), depend critically on aspects of the mating system (the preference function, mode of mate choice, choosiness, and number of potential mates sampled), the presence or absence of natural selection on the preferred trait, and the initial genetic parameters. Under some parameter combinations, preferential mating increased the heritability of the preferred trait, providing a possible resolution for the lek paradox. The Kirkpatrick–Barton approximation for r_G proved to be biased downward, but the realized genetic correlations were also low, generally <0.2. Such low values of r_G indicate that coevolution of the preference and preferred trait is likely to be very slow and subject to significant stochastic variation. Lande's model accurately predicted the incidence of runaway selection in the simulations, except where preferences were relative and the preferred trait was subject to natural selection. In these cases, runaways were over‐ or underestimated, depending on the number of males sampled. We conclude that rapid coevolution of preferences and preferred traits is unlikely in natural populations, but that the parameter combinations most conducive to it are most likely to occur in lekking species.     

An experimental test of mate choice for red carotenoid coloration in the marine copepod Tigriopus californicus

Colorful ornaments are hypothesized to have evolved in response to sexual selection for honest signals of individual quality that provide information about potential mates. Red carotenoid coloration is common in diverse groups, and in some vertebrate taxa, red coloration is a sexually selected trait whereby mates with the reddest ornaments are preferred . Despite being widespread among invertebrates, whether red carotenoid coloration is assessed during mate choice in these taxa is unclear. The marine copepod Tigriopus californicus displays red coloration from the accumulation of the carotenoid astaxanthin. Previous research on copepods has shown that astaxanthin provides protection from UV radiation and xenobiotic exposure and that carotenoid production is sensitive to external stressors. Because of the condition dependency of the red coloration, we hypothesized that Tigriopus would use it as a criterion during mate choice. To test this hypothesis, we conducted trials in which males chose between females that were wild-type red (carotenoid-rich algae diet) or white (carotenoid-deficient yeast diet). To control for dietary differences and to isolate the effect of carotenoid coloration, we also presented males with restored-red females fed a carotenoid-supplemented yeast diet. We found that wild-type red females were weakly preferred over white females. After controlling for diet, however, we found that restored-red females were avoided. Our observations do not support the hypothesis that male copepods prefer the carotenoid coloration of females during mate choice. We hypothesize that algal-derived compounds other than carotenoids play a role in mate choice. Red coloration in copepods appears to be a condition-dependent trait that is not assessed during mating.     

The evolution of female mating preferences: differentiation from species with promiscuous males can promote speciation

Females of many species are frequently courted by promiscuous males of their own and other closely related species. Such mating interactions may impose strong selection on female mating preferences to favor trait values in conspecific males that allow females to discriminate them from their heterospecific rivals. We explore the consequences of such selection in models of the evolution of female mating preferences when females must interact with heterospecific males from which they are completely postreproductively isolated. Specifically, we allow the values of both the most preferred male trait and the tolerance of females for males that deviate from this most preferred trait to evolve. Also, we consider situations in which females base their mating decisions on multiple male traits and must interact with males of multiple species. Females will rapidly differentiate in preference when they sometimes mistake heterospecific males for suitable mates, and the differentiation of female preference will select for conspecific male traits to differentiate as well. In most circumstances, this differentiation continues indefinitely, but slows substantially once females are differentiated enough to make mistakes rare. Populations of females with broader preference functions (i.e., broader tolerance for males with trait values that deviate from females' most preferred values) will evolve further to differentiate if the shape of the function cannot evolve. Also, the magnitude of separation that evolves is larger and achieved faster when conspecific males have lower relative abundance. The direction of differentiation is also very sensitive to initial conditions if females base their mate choices on multiple male traits. We discuss how these selection pressures on female mate choice may lead to speciation by generating differentiation among populations of a progenitor species that experiences different assemblages of heterospecifics. Opportunities for differentiation increase as the number of traits involved in mate choice increase and as the number of species involved increases. We suggest that this mode of speciation may have been particularly prevalent in response to the cycles of climatic change throughout the Quaternary that forced the assembly and disassembly of entire communities on a continentwide basis.     

Context‐ and State‐Dependent Male Mate Choice in a Sexually Cannibalistic Spider

High male mating investment may favor selection on male mate choice particularly if females vary in quality. Terminal investment strategies constitute a maximal mating effort and have evolved independently in the absence of paternal investment in several spider taxa including the genus Argiope. To test for male mate preferences in the above context, we used the sexually cannibalistic spider A. bruennichi. We varied male state (mating status and post‐maturation age) as well as the competitive context and quantified male mate choice decisions between females of different states and developmental stages in binary choice tests. We found an overall adaptive preference for the virgin against the mated female regardless of male mating state. Furthermore, we demonstrated that older males paid more attention to female fecundity‐related traits than to mating status. In a second set of experiments, we offered males a choice between a virgin and a subadult female and varied the competitive context which had no effect on male decisions. Curiously, a preference for the virgin adult female was only apparent after exclusion of females that matured <3 d prior to the test. Repeated tests of males supported the hypothesis that males do not distinguish between a freshly matured virgin female and a subadult female. Our results show that male spiders execute mate choice based on information collected from female silk strands and that they integrate their own state into mating 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.     

Aesthetic evolution by mate choice: Darwin's really dangerous 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.     

Female discrimination thresholds frequently exceed local male display variation: implications for mate choice dynamics and sexual selection

Among the factors that can influence female mate choice decisions is the degree to which females differentiate among similar displays: as differences decrease, females are expected to eventually stop discriminating. This discrimination threshold, in conjunction with the magnitude of male trait variation females regularly encounter while making mate choice decisions, may have important consequences for sexual selection. If local display variation is above the discrimination threshold, female preferences should translate into higher mating success for the more attractive male. But if display variation is frequently below the threshold, the resulting increased pattern of random mating may obscure the existence of female mate choice. I investigated the interplay between female discrimination and male display variation in green treefrogs (Hyla cinerea) and found that call trait differences between nearest neighbour males were frequently smaller than what females are expected to discriminate. This finding has two important consequences for our understanding of sexual selection in the wild: first, low display variation should weaken the strength of selection on male display traits, but the direction of selection should mirror the one predicted from females choice trials. Second, caution is needed when interpreting data on realized mating success in the wild: a pattern of random mating with respect to male display traits does not always mean that female preferences are weak or that conditions are too challenging for females to express their preferences. Rather, insufficient display variation can generate the same pattern.     

Evolution and genetic architecture of disassortative mating at a locus under heterozygote advantage

The evolution of mate choice is a major topic in evolutionary biology because it is thought to be a key factor in trait and species diversification. Here, we aim at uncovering the ecological conditions and genetic architecture enabling the puzzling evolution of disassortative mating based on adaptive traits. This rare form of mate choice is observed for some polymorphic traits but theoretical predictions on the emergence and persistence of this behavior are largely lacking. Thus, we developed a mathematical model to specifically understand the evolution of disassortative mating based on mimetic color pattern in the polymorphic butterfly Heliconius numata. We confirm that heterozygote advantage favors the evolution of disassortative mating and show that disassortative mating is more likely to emerge if at least one allele at the trait locus is free from any recessive deleterious mutations. We modeled different possible genetic architectures underlying mate choice behavior, such as self‐referencing alleles, or specific preference or rejection alleles. Our results showed that self‐referencing or rejection alleles linked to the color pattern locus enable the emergence of disassortative mating. However, rejection alleles allow the emergence of disassortative mating only when the color pattern and preference loci are tightly linked.     

Experience-mediated plasticity in mate preferences: mating assurance in a variable environment

An individual's prior experience of sexual signals can result in variation in mate preferences, with important consequences for the course of sexual selection. We test two hypotheses about the evolution of experience-mediated plasticity in mate preferences: mating assurance and mismating avoidance. We exposed female Enchenopa binotata treehoppers (Hemiptera: Membracidae) to treatments that varied their experience of signal frequency, the most divergent sexual signal trait in the E. binotata species complex. Treatments consisted of (1) signals matching the preferred frequency, (2-3) signals deviating either 100 Hz above or 100 Hz below the preferred frequency, and (4) no signals. Females experiencing preferred signals showed the greatest selectivity. However, experience had no effect on peak preference. These results support the hypothesis that selection has favored plasticity in mate preferences that ensures that mating takes place when preferred mates are rare or absent, while ensuring choice of preferred types when those are present. We consider how experience-mediated plasticity may influence selection on sexual advertisement signals, patterns of reproductive isolation, and the maintenance of genetic variation. We suggest that the plasticity we describe may increase the likelihood of successful colonization of a novel environment, where preferred mating types may be rare.     

Coevolution of costly mate choice and condition-dependent display of good genes.

Females often choose their mates, instead of mating at random, even when a father contributes nothing but genes to his offspring. Costly female preferences for males with exaggerated traits that reduce viability, such as the peacock's tail, are particularly puzzling. Such preferences can evolve if directly favoured by natural selection or when the exaggerated trait, although maladaptive per se, indicates high overall quality of the male's genotype. Two recent analyses suggested that the advantage to mate choice based on genetic quality is too weak to explain extreme cases of exaggeration of display traits and the corresponding preferences. We studied coevolution of a female mate-preference function and a genotype-dependent male display function where mutation supplies variation in genotype quality and mate preference is costly. Preference readily evolves, often causing extreme exaggeration of the display. Mate choice and trait expression can approach an equilibrium, or a limit cycle, or exaggeration can proceed forever, eventually causing extinction.     

The costs of choice in sexual selection

In Fisher's model of sexual selection female mating preferences are not subject to direct selection but evolve purely because they are genetically correlated with the favoured male trait. But when female choice is costly relative to random mating, for example in energy, time or predation risks, the evolution of female mating preference is subject also to direct selection. With costly female choice the set or line of equilibria found in models of Fisher's process no longer exists. On the line the male trait is under zero net selection, and there is no advantage for a female choosing a male with a more exaggerated character. Therefore any cost to choice causes choosiness to decline. In turn this lowers the strength of sexual selection and the male trait declines as well. So when Fisher's process is the sole force of sexual selection and female choice is costly, only transitory increases in female choice and the preferred male trait are possible. It has often been claimed that exaggerated male characters act as markers or revealers of the genetic quality of potential mates. If females choose their mates using traits that correlate with heritable viability differences then stable exaggeration of both female choice and the preferred male character is possible, even when female choice is costly. The offspring of choosy females have not only a Fisherian reproductive advantage but also greater viability. This suggests that in species with exaggerated male ornamentation, in which female choice is costly, it is likely that female mate choice will be for traits that correlate with male genetic quality.     

The evolution of reproductive character displacement conflicts with how sexual selection operates within a species

Processes that affect the evolution of female preferences or male display traits involved in mating decisions in different geographic areas have the potential to result in within-species divergence. This could occur via reinforcement of mate recognition in species using the same traits for species recognition and sexual selection. Sympatric individuals experience reinforcement of female preferences and male display traits, whereas allopatric individuals do not, creating the potential for divergent sexual selection in sympatric and allopatric populations. Sexual selection operates on the cuticular hydrocarbons (CHCs) of Drosophila serrata, and reinforcement on the CHCs of populations sympatric with D. birchii. Here, we manipulate sexual selection in D. serrata populations generated by hybridizing natural sympatric and allopatric populations. Under the influence of sexual selection, male CHCs evolved from an intermediate phenotype to resemble an allopatric phenotype, which was driven by female choice. Additionally, female choice resulted in evolution of an allopatric female preference, so that allopatric males were preferred to sympatric males. Allopatric CHCs and preferences represent a sexual selection optimum via female choice. Sympatric populations display suboptimal phenotypes relative to their allopatric conspecifics. The combination of reinforcement and sexual selection can therefore generate divergence in female preferences and male display traits.     

Assortative Pairings in Diamond Firetails (Stagonopleura guttata) are not the Result of Mutual Mate Choice for an Ornament

Positive assortative mating occurs when individuals with similar phenotypes mate more frequently with each other than is expected by chance. In species in which both the males and females are ornamented, assortative pairings could arise from mutual mate choice on the same trait. We test this mechanism of mate choice and assortative pairing in the Diamond Firetail (Stagonopleura guttata), an Australian estrildid finch in which both sexes are ornamented with red bills, red rumps and white flank spots. We have previously shown sex differences in the degree of ornamentation as females have more flank spots than males. These white flank spots are used during sexual display, being fully displayed by courting males and by females when approaching a displaying male. Here, we experimentally test whether mutual mate preference is based on the number of flank spots. There was no evidence for a direct mutual preference for spot number. Given a choice of potential mates with a natural or experimentally manipulated number of flank spots, males preferred females with more spots, while female preference was not solely based on flank spots. Intriguingly, in both wild and captive Diamond Firetails, we found the number of flank spots in pairs was correlated suggesting a basis for positive assortative pairing. Nevertheless, we conclude that assortative pairing in Diamond Firetails is not due to mutual choice of mates based on the number of flank spots. We discuss different selection pathways for this trait in each sex.     

Sounds different: inbreeding depression in sexually selected traits in the cricket Teleogryllus commodus

If male sexual signalling is honest because it captures genetic variation in condition then traits that are important mate choice cues should be disproportionately affected by inbreeding relative to other traits. To test this, we investigated the effect of brother-sister mating on advertisement calling by male field crickets Teleogryllus commodus. We quantified the effect of one generation of inbreeding on nightly calling effort and five finer-scale aspects of call structure that have been shown to influence attractiveness. We also quantified inbreeding depression on six life history traits and one morphological trait. Inbreeding significantly reduced hatching success, nymph survival and adult lifespan but had no detectable effect on hatching rate, developmental rate or adult body mass. The effect of inbreeding on sexually selected traits was equivocal. There was no decline in calling effort (seconds of sound production/night) by inbred males, but there were highly significant changes in three of five finer-scale call parameters. Sexually selected traits clearly vary in their susceptibility to inbreeding depression.     

GENETIC CORRELATIONS BETWEEN LIFE-HISTORY AND BEHAVIORAL TRAITS CAN CAUSE REPRODUCTIVE ISOLATION

Reproductive isolation may often evolve as an indirect (pleiotropic) consequence of populations adapting to different environments or habitats. For example, niches that are temporally or seasonally offset can select for organisms with different developmental characteristics. These developmental differences can inadvertently cause reproductive isolation by a variety of means including shifts in mating activity patterns. Here, we show a genetic correlation between a life-history trait (developmental period) and a behavioral trait (time of mating) that causes significant premating isolation in the melon fly, Bactrocera cucurbitae (Diptera: Tephritidae). Fly lines selected for short and long developmental periods differ in their preferred times of mating during the evening. This difference translates into significant prezygotic isolation, as measured by mate choice tests. If the time of mating between two populations differed more than one hour, the isolation index was significantly higher than zero. These indicate that premating isolation can be established if the developmental period is divergently selected for. If such genetic correlations are ubiquitous in many organisms, multifarious divergent selection for life-history traits would often accelerate the evolution of reproductive isolation. We speculate that reproductive isolation may have been evolved via genetic correlations among time-related traits, for example, developmental period and time of mating, as in other organisms.     

The scale‐of‐choice effect and how estimates of assortative mating in the wild can be biased due to heterogeneous samples

The mode in which sexual organisms choose mates is a key evolutionary process, as it can have a profound impact on fitness and speciation. One way to study mate choice in the wild is by measuring trait correlation between mates. Positive assortative mating is inferred when individuals of a mating pair display traits that are more similar than those expected under random mating while negative assortative mating is the opposite. A recent review of 1134 trait correlations found that positive estimates of assortative mating were more frequent and larger in magnitude than negative estimates. Here, we describe the scale‐of‐choice effect (SCE), which occurs when mate choice exists at a smaller scale than that of the investigator's sampling, while simultaneously the trait is heterogeneously distributed at the true scale‐of‐choice. We demonstrate the SCE by Monte Carlo simulations and estimate it in two organisms showing positive (Littorina saxatilis) and negative (L. fabalis) assortative mating. Our results show that both positive and negative estimates are biased by the SCE by different magnitudes, typically toward positive values. Therefore, the low frequency of negative assortative mating observed in the literature may be due to the SCE's impact on correlation estimates, which demands new experimental evaluation.     

The neural mechanisms of mate choice: a hypothesis

Scientists have described many physical and behavioral traits in avian and mammalian species that evolved to attract mates. But the brain mechanisms by which conspecifics become attracted to these traits is unknown. This paper maintains that two aspects of mate choice evolved in tandem: 1) traits that evolved in the "display producer" to attract mates and, 2) corresponding neural mechanisms in the "display chooser" that enable them to become attracted to these display traits. Then it discusses our (in-progress) fMRI brain scanning project on human romantic attraction, what we believe is a developed form of "courtship attraction" common to avian and mammalian species as well as the primary neural mechanism underlying avian and mammalian mate choice. The paper hypothesizes that courtship attraction is associated with elevated levels of central dopamine and norepinephrine and decreased levels of central serotonin in reward pathways of the brain. It also proposes that courtship attraction is part of a triune brain system for mating, reproduction and parenting. 1)The sex drive evolved to motivate birds and mammals to court any conspecifics. 2) The attraction system evolved to enable individuals to discriminate among potential mating partners and focus courtship activities on particular individuals, thereby conserving mating time and energy. 3) The neural circuitry for attachment evolved to enable individuals to complete species-specific parental duties.     

Direct fitness benefits explain mate preference,but not choice,for similarity in heterozygosity levels

Under sexual selection, mate preferences can evolve for traits advertising fitness benefits. Observed mating patterns (mate choice) are often assumed to represent preference, even though they result from the interaction between preference, sampling strategy and environmental factors. Correlating fitness with mate choice instead of preference will therefore lead to confounded conclusions about the role of preference in sexual selection. Here we show that direct fitness benefits underlie mate preferences for genetic characteristics in a unique experiment on wild great tits. In repeated mate preference tests, both sexes preferred mates that had similar heterozygosity levels to themselves, and not those with which they would optimise offspring heterozygosity. In a subsequent field experiment where we cross fostered offspring, foster parents with more similar heterozygosity levels had higher reproductive success, despite the absence of assortative mating patterns. These results support the idea that selection for preference persists despite constraints on mate choice.