A model for the evolution of assortative mating

Abstract: Many animals and plants show a correlation between the traits of the individuals in the mating pair, implying assortative mating. Given the ubiquity of assortative mating in nature, why and how it has evolved remain open questions. Here we attempt to answer these questions in those cases where the trait under assortment is the same in males and females. We consider the most favorable scenario for assortment to evolve, where the same trait is under assortment and viability selection. We find conditions for assortment to evolve using a multilocus formalism in a haploid population. Our results show how epistasis in fitness between the loci that control the focal trait is crucial for assortment to evolve. We then assume specific forms of assortment in haploids and diploids and study the limiting cases of selective and nonselective mating. We find that selection for increased assortment is weak and that where increased assortment is costly, it does not invade.     

Linking intra‐ and interspecific assortative mating: Consequences for asymmetric sexual isolation

Assortative mating is of interest because of its role in speciation and the maintenance of species boundaries. However, we know little about how within‐species assortment is related to interspecific sexual isolation. Most previous studies of assortative mating have focused on a single trait in males and females, rather than utilizing multivariate trait information. Here, we investigate how intraspecific assortative mating relates to sexual isolation in two sympatric and congeneric damselfly species (genus Calopteryx). We connect intraspecific assortment to interspecific sexual isolation by combining field observations, mate preference experiments, and enforced copulation experiments. Using canonical correlation analysis, we demonstrate multivariate intraspecific assortment for body size and body shape. Males of the smaller species mate more frequently with heterospecific females than males of the larger species, which showed less attraction to small heterospecific females. Field experiments suggest that sexual isolation asymmetry is caused by male preferences for large heterospecific females, rather than by mechanical isolation due to interspecific size differences or female preferences for large males. Male preferences for large females and male–male competition for high quality females can therefore counteract sexual isolation. This sexual isolation asymmetry indicates that sexual selection currently opposes a species boundary.     

Adaptive,but not condition‐dependent,body shape differences contribute to assortative mating preferences during ecological speciation

Assortative mating is critical for reproductive isolation during speciation; however, the mechanisms underlying mating preferences are often unknown. Assortative mating can be mediated through preferences for condition‐dependent and adaptive (“magic”) traits, but rigorously testing these hypotheses has been impeded by trait covariation in living organisms. We used computer‐generated models to examine the role of body shape in producing association preferences between fish populations undergoing ecological speciation in different habitat types. We demonstrate that body shape can serve as an adaptive trait (variation in head size between populations) and a condition‐dependent signal (variation in abdominal distention among individuals). Female preferences for stimuli varying in only one aspect of body shape uncovered evidence for body shape as a magic trait across population pairs, but no evidence for body shape serving as a condition‐dependent signal. Evolution of preferences only in females from one habitat type as well as stronger preferences in sympatric nonsulfidic as opposed to allopatric nonsulfidic populations suggests that reinforcement may have played a role in producing the observed patterns.     

Evolution of a mating preference for a dual‐utility trait used in intrasexual competition in genetically monogamous populations

The selection pressures by which mating preferences for ornamental traits can evolve in genetically monogamous mating systems remain understudied. Empirical evidence from several taxa supports the prevalence of dual‐utility traits, defined as traits used both as armaments in intersexual selection and ornaments in intrasexual selection, as well as the importance of intrasexual resource competition for the evolution of female ornamentation. Here, we study whether mating preferences for traits used in intrasexual resource competition can evolve under genetic monogamy. We find that a mating preference for a competitive trait can evolve and affect the evolution of the trait. The preference is more likely to persist when the fecundity benefit for mates of successful competitors is large and the aversion to unornamented potential mates is strong. The preference can persist for long periods or potentially permanently even when it incurs slight costs. Our results suggest that, when females use ornaments as signals in intrasexual resource competition, males can evolve mating preferences for those ornaments, illuminating both the evolution of female ornamentation and the evolution of male preferences for female ornaments in monogamous species.     

The relative importance of different direct benefits in the mate choices of a field cricket

Discussions about the evolution of female mating preferences have often suggested that females should express multiple strong preferences when different male traits are correlated with different mating benefits, yet few studies have directly tested this hypothesis by comparing the strength of female preferences for male traits known to be correlated with different benefits. In the variable field cricket, Gryllus lineaticeps, females receive fecundity and fertility benefits from mating with males with higher chirp rates and life-span benefits from mating with males with longer chirp durations. Although females prefer higher chirp rates and longer chirp durations when the other trait is held constant, it is possible that they give priority to one of these song traits when both vary. In this study, we examined the relative importance of chirp rate and chirp duration in female mate choice using single-stimulus presentations of songs that varied in both chirp rate and chirp duration. Females expressed both directional and stabilizing preferences based on chirp rate, responding most strongly to a chirp rate approximately one standard deviation above the population mean. Females did not express preferences based on chirp duration, and did not express correlational preferences. These results suggest that females may give priority to the reproductive benefits provided by males that produce higher chirp rates.     

Limits to the evolution of assortative mating by female choice under restricted gene flow

The evolution of assortative mating is a key component of the process of speciation with gene flow. Several recent theoretical studies have pointed out, however, that sexual selection which can result from assortative mating may cause it to plateau at an intermediate level; this is primarily owing to search costs of individuals with extreme phenotypes and to assortative preferences developed by individuals with intermediate phenotypes. I explore the limitations of assortative mating further by analysing a simple model in which these factors have been removed. Specifically, I use a haploid two-population model to ask whether the existence of assortative mating is sufficient to drive the further evolution of assortative mating. I find that a weakening in the effective strength of sexual selection with strong assortment leads to the existence of both a peak level of trait differentiation and the evolution of an intermediate level of assortative mating that will cause that peak. This result is robust to the inclusion of local adaptation and different genetic architecture of the trait. The results imply the existence of fundamental limits to the evolution of assortment via sexual selection in this situation, with which other factors, such as search costs, may interact.     

Sampling scale can cause bias in positive assortative mating estimates: evidence from two intertidal snails

Assortative mating in the wild is commonly estimated by correlating between traits in mating pairs (e.g. the size of males and females). Unfortunately, such an approach may suffer from considerable sampling bias when the distribution of different expressions of a trait in the wild is nonrandom (e.g. when segregation of different size classes of individuals occurs in different microhabitats or areas). Consequently, any observed trait correlation in the wild can be an artefact of pooling heterogeneous samples of mating pairs from different microhabitats or areas rather than true nonrandom matings. This bias in estimating trait correlations as a result of sampling scale is termed the scale‐of‐choice effect (SCE). In the present study, we use two intertidal littorinid species from Hong Kong to show how the SCE can bias size‐assortative mating estimates from mating pairs captured in the wild, empirically demonstrating the influence of this effect on measures of positive assortative mating. This finding cautions that studies overlooking the SCE may have misinterpreted the magnitude and the cause of assortative mating, and we provide a new analytical approach for protecting against this potential bias in future studies.     

The role of functional constraints in nonrandom mating patterns for a dance fly with female ornaments

Most hypotheses to explain nonrandom mating patterns invoke mate choice, particularly in species that display elaborate ornaments. However, conflicting selection pressures on traits can result in functional constraints that can also cause nonrandom mating patterns. We tested for functional load‐lifting constraints during aerial copulation in Rhamphomyia longicauda, a species of dance fly that displays multiple extravagant female‐specific ornaments that are unusual among sexual traits because they are under stabilizing selection. R. longicauda males provide females with a nuptial gift before engaging in aerial mating, and the male bears the entire weight of the female and nuptial gift for the duration of copulation. In theory, a male's ability to carry females and nuptial gifts could constrain pairing opportunities for the heaviest females, as reported for nonornamented dance flies. In concert with directional preferences for large females with mature eggs, such a load‐lifting constraint could produce the stabilizing selection on female size previously observed in this species. We therefore tested whether wild‐caught male R. longicauda collected during copulation were experiencing load‐lift limitations by comparing the mass carried by males during copulation with the male's wing loading traits. We also performed permutation tests to determine whether the loads carried by males during copulation were lighter than expected. We found that heavier males are more often found mating with heavier females suggesting that whereas R. longicauda males do not experience a load‐lift constraint, there is a strong relationship of assortative mating by mass. We suggest that active male mate choice for intermediately adorned females is more likely to be causing the nonrandom mating patterns observed in R. longicauda.     

Male mate preference as an agent of fecundity selection in a polymorphic salamander

Color polymorphisms are associated with variation in other traits which may affect individual fitness, and these color‐trait associations are expected to contribute to nonrandom mating in polymorphic species. The red‐backed salamander (Plethodon cinereus) exhibits a polymorphism in dorsal pattern: striped and unstriped, and previous studies have suggested that they may mate nonrandomly. However, the mechanism(s) contributing to this behavior remain unclear. Here we consider the role that male preference may have in driving mating behavior in P. cinereus. We limit our focus to striped individuals because this morph is most likely to be choosy given their dominant, aggressive behavioral profiles relative to unstriped males. Specifically, we evaluated (a) whether striped males preferentially associate with females with respect to her dorsum color, size, and body condition and (b) if so, whether female traits are evaluated via visual or chemical cues. We also considered whether the frequency of another male social behavior, nose taps, was associated with mate preferences. We found that striped male P. cinereus nose tapped more often to preferred females. However, males only assessed potential mates via chemical cues, preferring larger females overall. Reproductive phenology data on a sample of gravid females drawn from the same population indicated that the color morphs do not differ in reproductive traits, but larger females have greater fecundity. Given our findings, we conclude that female P. cinereus are under fecundity selection, mediated by male preference. In this manner, male mating behavior contributes to observations of nonrandom mate associations in this population of P. cinereus.     

Independent Mating Preferences for Male Body Size and Coloration in Female Trinidadian Guppies

Although females in numerous species generally prefer males with larger, brighter and more elaborate sexual traits, there is nonetheless considerable intra‐ and interpopulation variation in mating preferences amongst females that requires explanation. Such variation exists in the Trinidadian guppy, Poecilia reticulata, an important model organism for the study of sexual selection and mate choice. While female guppies tend to prefer more ornamented males as mates, particularly those with greater amounts of orange coloration, there remains variation both in male traits and female mating preferences within and between populations. Male body size is another trait that is sexually selected through female mate choice in some species, but has not been examined as extensively as body coloration in the guppy despite known intra‐ and interpopulation variation in this trait among adult males and its importance for survivorship in this species. In this study, we used a dichotomous‐choice test to quantify the mating preferences of female guppies, originating from a low‐predation population in Trinidad, for two male traits, body length and area of the body covered with orange and black pigmentation, independently of each other. We expected strong female mating preferences for both male body length and coloration in this population, given relaxation from predation and presumably relatively low cost of choice. Females indeed exhibited a strong preference for larger males as expected, but surprisingly a weaker (but nonetheless significant) preference for orange and black coloration. Interestingly, larger females demonstrated stronger preferences for larger males than did smaller females, which could potentially lead to size‐assortative mating in nature.     

Mating preference functions of individual female barking treefrogs, Hyla gratiosa, for two properties of male advertisement calls

Abstract.— A mating preference function describes the relationship between variation in a trait in potential mates and the strength of the preference for that trait. Few studies have measured mating preference functions either at a population level or for individuals. We used two-choice playback experiments to determine the mating preference functions of individual female barking treefrogs for two call characteristics: call-repetition rate and fundamental frequency. We tested each female four times with each pair of stimuli and with three to six pairs of stimuli. Individual females exhibited directional preferences for higher call rates and stabilizing preferences for intermediate fundamental frequency. These individual preference functions were similar to population-level preferences documented in previous studies. Within a stimulus type (call rate or fundamental frequency), nearly all females exhibited the same general preference function. However, females varied in the minimum difference between stimuli necessary to elicit a unanimous choice for the higher call rate, and they differed in both the intermediate fundamental frequency they preferred most and the minimum difference in fundamental frequency that elicited a unanimous choice for one of the two alternatives. The variation we observed among females was not repeatable; repeatabilities were in general low and statistically nonsignificant. The observed variation in the preferences of females, even if unrepeatable, should weaken selection on male traits relative to selection in the absence of such variation.     

Frequency-dependent selection and the evolution of assortative mating

A long-standing goal in evolutionary biology is to identify the conditions that promote the evolution of reproductive isolation and speciation. The factors promoting sympatric speciation have been of particular interest, both because it is notoriously difficult to prove empirically and because theoretical models have generated conflicting results, depending on the assumptions made. Here, we analyze the conditions under which selection favors the evolution of assortative mating, thereby reducing gene flow between sympatric groups, using a general model of selection, which allows fitness to be frequency dependent. Our analytical results are based on a two-locus diploid model, with one locus altering the trait under selection and the other locus controlling the strength of assortment (a "one-allele" model). Examining both equilibrium and nonequilibrium scenarios, we demonstrate that whenever heterozygotes are less fit, on average, than homozygotes at the trait locus, indirect selection for assortative mating is generated. While costs of assortative mating hinder the evolution of reproductive isolation, they do not prevent it unless they are sufficiently great. Assortative mating that arises because individuals mate within groups (formed in time or space) is most conducive to the evolution of complete assortative mating from random mating. Assortative mating based on female preferences is more restrictive, because the resulting sexual selection can lead to loss of the trait polymorphism and cause the relative fitness of heterozygotes to rise above homozygotes, eliminating the force favoring assortment. When assortative mating is already prevalent, however, sexual selection can itself cause low heterozygous fitness, promoting the evolution of complete reproductive isolation (akin to "reinforcement") regardless of the form of natural selection.     

Mating Success in the Polyandrous Social Wasp Vespula maculifrons

The mating decisions made by social insect males and females profoundly affect the structure of colonies and populations. However, few studies have used experimental approaches to understand mating behavior and mate choice in social insect taxa. This study investigated mating success in the polyandrous social wasp Vespula maculifrons. Mating trials were designed to test predictions that characteristics of body size and colony‐of‐origin would affect mating success. We first investigated if size differences existed among individuals and found that males from different colonies differed significantly in the size of nine morphological traits. However, male trait size was not significantly associated with male mating success. In contrast, females from different colonies differed significantly in only six of the nine measured traits, and four of these traits were associated with successful mating behaviors. Specifically, the correlated traits of gaster length, third tergum length, antennal length, and total length were positively associated with female mating success. Thus, long females experience mating advantages over females that are short. We also found that males and females from one particular colony displayed significantly greater mating activity than individuals from other colonies. Thus, the colony from which individuals originate plays an important role in determining mating success. Finally, our experiments failed to detect any evidence of nestmate avoidance during the mating trials. Overall, our data suggest that social insect reproductives may experience differential mating success based on their phenotype or developmental environment.     

Defining the genetic architecture underlying female- and male-mediated nonrandom mating and seed yield traits in Arabidopsis

Postpollination nonrandom mating among compatible mates is a widespread phenomenon in plants and is genetically undefined. In this study, we used the recombinant inbred line (RIL) population between Landsberg erecta and Columbia (Col) accessions of Arabidopsis (Arabidopsis thaliana) to define the genetic architecture underlying both female- and male-mediated nonrandom mating traits. To map the genetic loci responsible for male-mediated nonrandom mating, we performed mixed pollinations with Col and RIL pollen on Col pistils. To map the genetic loci responsible for female-mediated nonrandom mating, we performed mixed pollinations with Col and Landsberg erecta pollen on RIL pistils. With these data, we performed composite interval mapping to identify two quantitative trait loci (QTLs) that control male-mediated nonrandom mating. We detected epistatic interactions between these two loci. We also explored female- and male-mediated traits involved in seed yield in mixed pollinations. We detected three female QTLs and one male QTL involved in directing seed number per fruit. To our knowledge, the results of these experiments represent the first time the female and male components of seed yield and nonrandom mating have been separately mapped.     

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.     

Direct and indirect assortative mating: a multivariate approach to plant flowering schedules

This paper develops methods to partition the phenotypic correlation between mates for a focal trait--the standard measure for assortative mating--into a direct component and additional indirect components. Indirect assortative mating occurs when a nonassorting trait is correlated within individuals to a directly assorting trait. Direct and indirect assortative mating is assessed for flowering phenology in Brassica rapa. The flowering time of pollen recipients (mothers) was strongly correlated (rho=0.67) to that of potential pollen donors (fathers). Similarly, recipients and donors were correlated for duration of their flowering periods (rho=0.32) and stem diameters (rho=0.52). A partitioning of between-mate correlations revealed direct assortative mating for flowering time and period duration. However, assortment for stem diameter is explained solely through its correlation to flowering time. Examination of standard quantitative genetic theory shows that indirect assortative mating inflates genetic variance in a focal trait and the genetic covariance between focal and phenotypically correlated traits.     

MATE PREFERENCE FOR A PHENOTYPICALLY PLASTIC TRAIT IS LEARNED,AND MAY FACILITATE PREFERENCE‐PHENOTYPE MATCHING

Fixed, genetically determined, mate preferences for species whose adult phenotype varies with rearing environment may be maladaptive, as the phenotype that is most fit in the parental environment may be absent in the offspring environment. Mate preference in species with polyphenisms (environmentally dependent alternative phenotypes) should therefore either not focus on polyphenic traits, be polyphenic themselves, or learned each generation. Here, we test these alternative hypotheses by first describing a female‐limited seasonal polyphenism in a sexually dimorphic trait in the butterfly Bicyclus anynana, dorsal hindwing spot number (DHSN), and then testing whether male and female mate preferences for this trait exist, and whether they are seasonally polyphenic, or learned. Neither naïve males nor naïve females in either seasonal form exhibited mating preferences for DHSN. However, males, but not females, noticed DHSN variation and learned mate preferences for DHSN. These results suggest that individuals may accommodate environmentally dependent variation in morphological traits via learned mate preferences in each generation, and that learned mate preference plasticity can be sexually dimorphic.     

Evolution of assortative mating in a population expressing dominance

In this article, we study the influence of dominance on the evolution of assortative mating. We perform a population-genetic analysis of a two-locus two-allele model. We consider a quantitative trait that is under a mixture of frequency-independent stabilizing selection and density- and frequency-dependent selection caused by intraspecific competition for a continuum of resources. The trait is determined by a single (ecological) locus and expresses intermediate dominance. The second (modifier) locus determines the degree of assortative mating, which is expressed in females only. Assortative mating is based on similarities in the quantitative trait ('magic trait' model). Analytical conditions for the invasion of assortment modifiers are derived in the limit of weak selection and weak assortment. For the full model, extensive numerical iterations are performed to study the global dynamics. This allows us to gain a better understanding of the interaction of the different selective forces. Remarkably, depending on the size of modifier effects, dominance can have different effects on the evolution of assortment. We show that dominance hinders the evolution of assortment if modifier effects are small, but promotes it if modifier effects are large. These findings differ from those in previous work based on adaptive dynamics.     

A Behavioral Syndrome in the Adzuki Bean Beetle: Genetic Correlation Among Death Feigning,Activity, and Mating Behavior

When studying animal behavior, it is often necessary to examine traits as a package, rather than as isolated units. Evidence suggests that individuals behave in a consistent manner across different contexts or over time; that is, behavioral syndromes. We compared locomotor activity levels and mating success between beetles derived from two regimes artificially selected for the duration of death‐feigning behavior in the adzuki bean beetle, Callosobruchus chinensis. The two selection regimes comprised strains with higher (L) and lower (S) intensity (frequency and duration) of death‐feigning behavior, respectively. We found that S strains had higher activity levels than L strains for both sexes, i.e., there is a negative genetic correlation between death feigning and activity. In addition, we found that S strains had higher mating success than L strains, presumably due to higher activity, in males but not in females. We thus demonstrate that death feigning is genetically correlated to mating behavior in males but not females in this species, suggesting that behavioral correlations may not always reflect in the same way in both sexes.     

Assortative Mating and Lack of Temporality Between Corn and Rice Strains of Spodoptera frugiperda (Lepidoptera,Noctuidae) from Central Colombia

Spodoptera frugiperda is a Neotropical moth that has diverged into “corn” and “rice” strains. In the US, prezygotic isolation studies have shown that both populations mate assortatively. In addition, recent studies have demonstrated that mating by the same strain individuals is enhanced by an allochronic shift in mating activity and male pheromones are important during courtship. In Colombia, studies on mate choice have never been performed previously, although earlier analyses made in populations from Central Colombia showed no significant differences in time of first mating and copula duration between the strains. Here, we performed multiple choice experiments using a tetrad design composed of individuals of the corn and the rice strains. We found that corn strain females rarely mate with rice strain males, but rice strain females mate with both strains of males. In addition, no temporal isolation was found. A ML (maximum likelihood) approach was used to discriminate between mating propensity and mate choice behaviors in S. frugiperda strains. This approach showed that mating propensity of corn strain males is three times greater than rice strain males. In contrast, in females, the propensity of mating was slightly higher for the corn strain. Finally, the isolation index between the corn and the rice strains from Colombia produced a value of I?=?0.33. Our results suggest that prezygotic isolation at the behavioral and temporal levels differ between the US and Colombia. Moreover, in the US temporal isolation appears to have an important role in behavioral isolation but in Colombia temporality is not necessary to reduce encounters between S. frugiperda strains.