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.     

On the Relative Importance of Haplo-Diploidy, Assortative Mating and Social Synergy on the Evolutionary Emergence of Social Behavior

Advances in multiagent simulation techniques make it possible to study more realistic dynamics of complex systems and allow evolutionary theories to be tested. Here I use simulations to assess the relative importance of reproductive systems (haplodiploidy vs. diploidy), mate selection (assortative mating vs. random mating) and social economics (pay-off matrices of evolutionary games) in the evolutionary dynamics leading to the emergence of social cooperation in the provision of parental care. The simulations confirm that haplo-diploid organisms and organisms mating assortatively have a higher probability for fixing alleles and require less favorable conditions for their fixation, than diploids or organisms mating randomly. The simulations showed that social behavior was most likely to emerge a) when the cost for parental investment was much lower than the benefits to the offspring, b) when cooperation improved synergistically the fitness of offspring compared to the corresponding egoistic behavior and c) when alleles coding for altruistic or social behavior could be rapidly fixed in the population, thanks to mechanisms such as haplo-diploidy and/or assortative mating. Cooperative social behavior always appeared if sociality conferred much higher fitness gains compared to non cooperative alternatives suggesting that the most important factors for the emergence and maintenance of social behavior are those based on energetic or efficiency considerations. The simulations, in congruence with the scant experimental evidence available, suggest that economic considerations rather than genetic ones are critical in explaining the emergence and maintenance of sociality.     

The Effect of Assortative Mating on the Coexistence of a Hybridogenetic Waterfrog and Its Sexual Host

In central Europe, the hybridogenetic waterfrog Rana esculenta, a hybrid between Rana ridibunda and Rana lessonae, lives in sympatry with one of its parental species, the poolfrog Rana lessonae. As R. esculenta has to backcross constantly with R. lessonae in order to produce viable offspring, this coexistence is obligatory for R. esculenta. Since R. esculenta has a higher primary fitness than R. lessonae, a mechanism is required that prevents the hybrid from driving the parental species, and hence itself, to extinction. Here, we present an analytical model and a computer simulation that investigate whether assortative mating can operate as a such a control mechanism. Our results show that assortative mating is very effective in regulating coexistence in such a hybrid-host system. This is particularly true when choice is affected by the proportion of the two male types in the population. Furthermore, we could show that even if the species composition in a mixed hybrid-host population may be largely influenced by differences in life-history parameters, assortative mating still plays a very important role by stabilizing coexistence. Thus, mating behavior turns out to be more important for the populations dynamics of hybridogenetic waterfrog systems than previously assumed.     

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.     

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.     

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 effect of positive assortative mating on genetic parameters in a simulated beef cattle population

Summary Two simulated data sets, representing random mating and positive assortative mating in a beef cattle population over 10 rounds of mating, were each composed of 100 replicates. Three correlated traits were considered; calving ease (CE), 200 day weight (WW) and postweaning gain (PG). All selection practiced in the simulation was random. Positive assortative mating, which was based on parental WW phenotypic records, increased the progeny additive genetic variance of WW. The absolute values of genetic covariances and correlations between WW with CE and PG were also increased by positive assortative mating. Variances or covariances did not reach their expected equilibrium values due to overlapping generations, low replacement rates and only 10 rounds of mating.The financial assistance of Agriculture Canada and the Natural Sciences and Engineering Research Council of Canada are gratefully acknowledged     

The effect of positive assortative mating at one locus on a second linked locus

Summary A model for positive assortative mating based on genotype for one locus is employed to investigate the effect of this mating system on the genotypic structure of a second linked locus as well as on the joint genotypic structure of these two loci. It is shown that the second locus does not attain a precise positive assortative mating structure, but yet it shares a property that is characteristic of positive assortative mating, namely an increase in the frequency of homozygotes over that typically found in panmictic structures. Given any arbitrary genotypic structure for the parental population, the resulting offspring generation possesses a structure at the second locus that does not depend on the recombination frequency, while the joint structure of course does. In case assortative mating as well as linkage are not complete, there exists a unique joint equilibrium state for the two loci, which is characterized by complete stochastic independence between the two loci as well as by Hardy-Weinberg proportions at the second locus. For the second locus alone, Hardy-Weinberg equilibrium is realized if and only if gametic linkage equilibrium and an additionally specified condition are realized.     

THE COADAPTATION OF PARENTAL AND OFFSPRING CHARACTERS

Parents often have important influences on their offspring's traits and/or fitness (i.e., maternal or paternal effects). When offspring fitness is determined by the joint influences of offspring and parental traits, selection may favor particular combinations that generate high offspring fitness. We show that this epistasis for fitness between the parental and offspring genotypes can result in the evolution of their joint distribution, generating genetic correlations between the parental and offspring characters. This phenomenon can be viewed as a coadaptive process in which offspring genotypes evolve to function with the parentally provided environment and, in turn, the genes for this environment become associated with specific offspring genes adapted to it. To illustrate this point, we present two scenarios in which selection on offspring alone alters the correlation between a maternal and an offspring character. We use a quantitative genetic maternal effect model combined with a simple quadratic model of fitness to examine changes in the linkage disequilibrium between the maternal and offspring genotypes. In the first scenario, stabilizing selection on a maternally affected offspring character results in a genetic correlation that is opposite in sign to the maternal effect. In the second scenario, directional selection on an offspring trait that shows a nonadditive maternal effect can result in selection for positive covariances between the traits. This form of selection also results in increased genetic variation in maternal and offspring characters, and may, in the extreme case, promote host-race formation or speciation. This model provides a possible evolutionary explanation for the ubiquity of large genetic correlations between maternal and offspring traits, and suggests that this pattern of coinheritance may reflect functional relationships between these characters (i.e., functional integration).     

ASSORTATIVE MATING PREFERENCES AMONG HYBRIDS OFFERS A ROUTE TO HYBRID SPECIATION

Homoploid speciation generates species without a change in chromosome number via introgressive hybridization and has been considered rare in animals. Heliconius butterflies exhibit bright aposematic color patterns that also act as cues in assortative mating. Heliconius heurippa has a color pattern that can be recreated by introgression of the H. melpomene red band into an H. cydno genetic background. Wild H. heurippa males show assortative mating based on color pattern and we here investigate the origin of this preference by studying first-generation backcross hybrids between H. melpomene and H. cydno that resemble H. heurippa . These hybrids show assortative mating preferences, showing a strong preference for their own color pattern over that of either parental species. This is consistent with a genetic basis to wing pattern preference and implies, first, that assortative mating preferences would facilitate the initial establishment of a homozygous hybrid color pattern by increasing the likelihood that early generation hybrids mate among themselves. Second, once established such a lineage would inherit assortative mating preferences that would lead to partial reproductive isolation from parental lineages.     

Mating frequency and inclusive fitness in Drosophila melanogaster

In many species, increased mating frequency reduces maternal survival and reproduction. In order to understand the evolution of mating frequency, we need to determine the consequences of increased mating frequency for offspring. We conducted an experiment in Drosophila melanogaster in which we manipulated the mating frequency of mothers and examined the survival and fecundity of the mothers and their daughters. We found that mothers with the highest mating frequency had accelerated mortality and more rapid reproductive senescence. On average, they had 50% shorter lives and 30% lower lifetime reproductive success (LRS) than did mothers with the lowest mating frequency. However, mothers with the highest mating frequency produced daughters with 28% greater LRS. This finding implies that frequent mating stimulates cross-generational fitness trade-offs such that maternal fitness is reduced while offspring fitness is enhanced. We evaluate these results using a demographic metric of inclusive fitness. We show that the costs and benefits of mating frequency depend on the growth rate of the population. In an inclusive fitness context, there was no evidence that increased mating frequency results in fitness costs for mothers. These results indicate that cross-generational fitness trade-offs have an important role in sexual selection and life-history evolution.     

Models of multifactorial inheritance: II, the covariance structure for a scalar phenotype under selective assortative mating and sex-dependent symmetric parental-transmission

This study concentrates on a scalar trait for a two-sex population entailing symmetric sex-dependent parent-offspring transmission, a nonlinear (selective) assortative mating pattern, and random perturbation factors. A number of qualitative and comparative properties of the equilibrium covariance structure are set forth. In particular, it is shown that the phenotype variance generally increases under attenuated assortative mating tendencies and for an increased level of parent-offspring transmission. Moreover, with more contrasting sex-dependent transmission the sibling covariances diverge from the parent-offspring covariance. Also, shared residual-environmental covariance enhances the sibling covariances. The absolute product moment of the deviation of a child phenotype from the separate parental phenotypes exhibits a minimum for a mixed assortative random mating scheme rather than under extreme assortative mating or pure random mating. We establish that the equilibrium variance of a married individual is reduced compared to the variance of the population at large. Interpretations and implications are discussed.     

The genetic architecture of ecological specialization: correlated gene effects on host use and habitat choice in pea aphids

Genetic correlations among phenotypic characters result when two traits are influenced by the same genes or sets of genes. By reducing the degree to which traits in two environments can evolve independently (e.g., Lande 1979; Via and Lande 1985), such correlations are likely to play a central role in both the evolution of ecological specialization and in its link to speciation. For example, negative genetic correlations between fitness traits in different environments (i.e., genetic trade-offs) are thought to influence the evolution of specialization, while positive genetic correlations between performance and characters influencing assortative mating can accelerate the evolution of reproductive isolation between ecologically specialized populations. We first discuss how the genetic architecture of a suite of traits may affect the evolutionary role of genetic correlations among them and review how the mechanisms of correlations can be analyzed using quantitative trait locus (QTL) mapping. We then consider the implications of such data for understanding the evolution of specialization and its link to speciation. We illustrate this approach with a QTL analysis of key characters in two races of pea aphids that are highly specialized on different host plants and partially reproductively isolated. Our results suggest that antagonism among QTL effects on performance in the two environments leads to a genetic trade-off in this system. We also found evidence for parallel QTL effects on host-plant acceptance and fecundity on the accepted host, which could produce assortative mating. These results suggest that the genetic architecture of traits associated with host use may have played a central role in the evolution of specialization and reproductive isolation in pea aphids.     

Demographic influences of translocated individuals on a resident population of house sparrows

Translocation of individuals from source populations to augment small populations facing risk of extinction is an important conservation tool. Here we examine sex‐specific differences between resident and translocated house sparrows Passer domesticus in reproductive success and survival, and the contribution of translocated individuals to the growth of a local population. We found evidence for assortative mating based on origin revealed by fewer parentages between translocated males and resident females than expected, and the total number of fledglings produced by such pairs was lower. The reproductive success of translocated males was positively related to the size of the throat badge (a sexual ornament), such that only translocated males with a large badge size were as successful as resident males. However, offspring with parents of different origin had higher survival than offspring with parents of the same origin, which suggests hybrid vigour. The contribution of resident and translocated individuals to the stochastic component of the long‐run growth rate of the population was similar; neither the mean individual contributions in fitness nor the demographic variance differed between the two groups. Thus, this experiment shows that translocated individuals may have a similar demographic influence on the growth of local populations as resident individuals. Still, the intermixing of translocated and resident individuals was low, and fitness differed according to origin in relation to individual differences in a sexually selected trait. In addition, hybrid vigour with respect to offspring recruitment seemed to partially decrease the negative fitness consequences of the assortative mating based on origin.     

The evolutionary history of Drosophila buzzatii. XX. Positive phenotypic covariance between field adult fitness components and body size

In the cactophilic species Drosphila buzzatii, it is feasible to infer the action of natural selection by simultaneously sampling different life history stages in the field. During four years of research, samples of mating and non-mating adults and pupae were taken from a natural population. The main adult fitness components, i.e., mating success, longevity, and fecundity, were recorded in relation to body size, as measured by thorax length. The age of flies was estimated by observing the developmental stage of the reproductive system. Our data showed that larger flies can outlive and outmate small flies, and that mating success is related to age. An estimate of the fitness function showed a linear increase of mating success with increasing thorax length. There was no assortative mating for this trait. We advance the hypothesis that mating success is related to the rate of encounter and courtship time through general activity, which in turn may be related to body size. A positive phenotypic correlation between thorax length and ovariole number, which is related to fecundity, was found in females emerged from wild pupae. Neither the phenotypic nor the genetic (additive) correlations between these two traits were statistically different from zero in laboratory reared females. The genetic consequences of the observed phenotypic selection on body size are discussed.     

Simulating the extinction of parental lineages from introgressive hybridization: the effects of fitness,initial proportions of parental taxa,and mate choice

Genomic introgression among divergent taxa following human-mediated secondary contact is a growing concern for the management and conservation of aquatic biodiversity. We simulated the composition of taxa following admixture and hybridization by independently altering three variables: (1) initial proportion of parental taxa following secondary contact; (2) fitness gradients among parental and introgressant taxa; and, (3) strength of assortative mating among these taxa. Ultimately, we established that parental taxa will trend toward extinction as introgression proceeds in spite of even a heavy fitness penalty for the hybrids. Also, the number of generations required (rate) to reach an arbitrarily determined threshold of extinction (< 5.0%) was inversely related to the strength of the relative fitness gradients among parental and derivative hybridized lineages. Moreover, the rates of extinction for parental taxa depended on the initial relative proportions in the admixture with rare taxa going extinct more rapidly than abundant taxa. Finally, the strength of assortative mating (as an evolved or reinforced mechanism of pre-mating isolation) will affect the rate of extinction. Introgressive hybridization, therefore, emerges as an important risk to structural biodiversity wherever divergent, yet reproductively compatible, taxa come together naturally or are brought together through human activities.     

Morph‐dependent fitness and directional change of morph frequencies over time in a Dutch population of Common buzzards Buteo buteo

How genetic polymorphisms are maintained in a population is a key question in evolutionary ecology. Previous work on a plumage colour polymorphism in the common buzzard Buteo buteo suggested heterozygote advantage as the mechanism maintaining the co‐existence of three morphs (light, intermediate and dark). We took advantage of 20 years of life‐history data collected in a Dutch population to replicate earlier studies on the relationship between colour morph and fitness in this species. We examined differences between morphs in adult apparent survival, breeding success, annual number of fledglings produced and cumulative reproductive success. We found that cumulative reproductive success differed among morphs, with the intermediate morph having highest fitness. We also found assortative mating for colour morph, whereby assortative pairs were more likely to produce offspring and had longer‐lasting pair bonds than disassortative pairs. Over the 20‐year study period, the proportion of individuals with an intermediate morph increased. This apparent evolutionary change did not just arise from selection on individual phenotypes, but also from fitness benefits of assortative mating. The increased frequency of intermediates might also be due to immigration or drift. We hypothesize that genetic variation is maintained through spatial variation in selection pressures. Further studies should investigate morph‐dependent dispersal behaviour and habitat choice.     

The perceived benefits of height: strength, dominance, social concern, and knowledge among Bolivian native Amazonians

Research in industrial countries suggests that, with no other knowledge about a person, positive traits are attributed to taller people and correspondingly, that taller people have slightly better socioeconomic status (SES). However, research in some non-industrialized contexts has shown no correlation or even negative correlations between height and socioeconomic outcomes. It remains unclear whether positive traits remain attributed to taller people in such contexts. To address this question, here we report the results of a study in a foraging-farming society of native Amazonians in Bolivia (Tsimane')--a group in which we have previously shown little association between height and socioeconomic outcomes. We showed 24 photographs of pairs of Tsimane' women, men, boys, and girls to 40 women and 40 men >16 years of age. We presented four behavioral scenarios to each participant and asked them to point to the person in the photograph with greater strength, dominance, social concern, or knowledge. The pairs in the photographs were of the same sex and age, but one person was shorter. Tsimane' women and men attributed greater strength, dominance, and knowledge to taller girls and boys, but they did not attribute most positive traits to taller adults, except for strength, and more social concern only when women assessed other women in the photographs. These results raise a puzzle: why would Tsimane' attribute positive traits to tall children, but not tall adults? We propose three potential explanations: adults' expectations about the more market integrated society in which their children will grow up, height as a signal of good child health, and children's greater variation in the traits assessed corresponding to maturational stages.     

PARTITIONING THE EFFECTS OF SPATIAL ISOLATION,NEST HABITAT,AND INDIVIDUAL DIET IN CAUSING ASSORTATIVE MATING WITHIN A POPULATION OF THREESPINE STICKLEBACK

Assortative mating is measured as a phenotypic or genotypic correlation between mates. Although biologists typically view assortative mating in terms of mate preference for similar partners, correlations between mates can also arise from phenotypic spatial structure arising from spatial isolation or habitat preferences. Here, we test whether diet‐assortative mating within an ecologically variable population of threespine stickleback results from small‐scale geographic isolation or microhabitat preference. We find evidence for assortative mating in the form of a positive correlation between mated pairs’ diets (measured using stable isotopes). Stable isotopes reveal diet differences between different nesting areas and among individuals using different nest habitat within a nesting area. This spatial segregation of diet types should generate some assortative mating, but is insufficient to explain the observed assortment strength. Significant male–female isotope correlations remain after controlling for spatial variables. We therefore conclude that sticklebacks’ diet‐assortative mating arises from additional behavioral preference. More generally, our results illustrate the point that spatial segregation can only drive appreciable levels of phenotypic assortative mating when environment‐phenotype correlations are parallel and strong in both sexes. Consequently, intraspecific assortative mating may typically entail mating preferences rather than just spatial cosegregation of phenotypes.