Maria R Servedio

University of North Carolina at Chapel Hill | UNC · Department of Biology

Egg rejection is an effective and widespread antiparasitic defense to eliminate foreign eggs from the nests of hosts of brood parasitic birds. Several lines of observational and critical experimental evidence support a role for learning by hosts in the recognition of parasitic versus own eggs; specifically, individual hosts that have had prior or c...

Predation plays a role in preventing the evolution of ever more complicated sexual displays, because such displays often increase an individual's predation risk. Sexual selection theory, however, omits a key feature of predation in modeling costs to sexually selected traits: Predation is density dependent. As a result of this density dependence, pr...

Wild populations suffer two types of stochasticity: demographic stochasticity, from sampling error in offspring number, and environmental stochasticity, from temporal variation of the growth rate. By modeling evolution through phenotypic selection following an abrupt environmental change, we investigate how genetic and demographic dynamics, as well...

Upon the secondary contact of populations, speciation with gene flow is greatly facilitated when the same pleiotropic loci are both subject to divergent ecological selection and induce non-random mating, leading to loci with this fortuitous combination of functions being referred to as 'magic trait' loci. We use a population genetics model to exami...

Sexual selection has a rich history of mathematical models that consider why preferences favor one trait phenotype over another (for population genetic models) or what specific trait value is preferred (for quantitative genetic models). Less common is exploration of the evolution of choosiness or preference strength: that is, by how much a trait is...

Upon the secondary contact of populations, speciation with gene flow is greatly facilitated when the same pleiotropic loci are both subject to divergent ecological selection and induce non-random mating, leading to loci with this fortuitous combination of functions being referred to as "magic trait" loci. We use a population genetics model to exami...

The presence of same-sex sexual behavior across the animal kingdom is often viewed as unexpected. One explanation for its prevalence in some taxa is indiscriminate mating-a strategy wherein an individual does not attempt to determine the sex of its potential partner before attempting copulation. Indiscriminate mating has been argued to be the ances...

Despite widespread interest in the evolution and implications of monogamy across taxa, less attention—especially theoret-ical—has been paid toward understanding the evolution of divorce (ending a socially monogamous pairing to find a new partner). Here, we develop a model of the evolution of divorce by females in a heterogeneous environment, where...

Influential models of speciation by sexual selection posit either a single shared preference for a universal display, expressed only when males are locally adapted and hence in high condition, or that shared loci evolve population-specific alleles for displays and preferences. However, many closely related species instead show substantial differenc...

The strength of mate choice (choosiness) often varies with age, but theory to understand this variation is scarce. Additionally, theory has investigated the evolution of choosiness in speciation scenarios but has ignored that most organisms have overlapping generations. We investigate whether speciation can result in variation of choosiness with ag...

Pollination requires a flower to remain open for long enough to allow for the arrival of pollinators. However, maintaining flowers costs energy and resources. Therefore, flower longevity, the length of time a flower remains viable, is critical for the outcome of plant reproduction. Although previous studies showed that the evolution of flower longe...

If there are no constraints on the process of speciation, then the number of species might be expected to match the number of available niches and this number might be indefinitely large. One possible constraint is the opportunity for allopatric divergence. In 1981, Felsenstein used a simple and elegant model to ask if there might also be genetic c...

The widespread presence of same-sex sexual behaviour (SSB) has long been thought to pose an evolutionary conundrum, as participants in SSB suffer the cost of failing to reproduce after expending the time and energy to find a mate. The potential for SSB to occur as part of an optimal strategy has received less attention, although indiscriminate sexu...

The widespread presence of same-sex sexual behavior (SSB) has long been thought to pose an evolutionary conundrum [1-3], as participants in SSB suffer the cost of failing to reproduce after expending the time and energy to find a mate. The potential for SSB to occur as part of an optimal strategy has received almost no attention, although indiscrim...

“Magic traits”, in which the same trait is both under divergent ecological selection and forms the basis of assortative mating, have been sought after due to their supposed unique ability to promote divergence with gene flow. Here we ask how unique magic traits are, by exploring whether a tightly linked complex of a locus under divergent selection...

Decades of theoretical work on the evolution of adaptive prezygotic isolation have led to an interesting finding – namely that stable partial reproductive isolation is a relatively common outcome. This conclusion is generally lost, however, in the desire to pinpoint when exactly speciation occurs. Here we argue that the evolution of partial reprodu...

In many species that form pair bonds, males display to their mate after pair formation. These displays elevate the female’s investment into the brood. This is a form of cooperation because without the display, female investment is reduced to levels that are suboptimal for both sexes. The presence of such displays is paradoxical as in their absence...

Theoretical models often have fundamentally different goals than do empirical studies of the same topic. Models can test the logic of existing hypotheses, explore the plausibility of new hypotheses, provide expectations that can be tested with data, and address aspects of topics that are currently inaccessible empirically. Theoretical models are co...

Sexual imprinting—a phenomenon in which offspring learn parental traits and later use them as a model for their own mate preferences—can generate reproductive barriers between species¹. When the target of imprinting is a mating trait that differs among young lineages, imprinted preferences may contribute to behavioural isolation and facilitate spec...

Sexual selection has long been acknowledged as an important evolutionary force, capable of shaping phenotypes ranging from fascinating and unusual displays to cryptic traits whose function is only uncovered by careful study. Yet, despite decades of research, reaching a consensus definition of the term 'sexual selection' has proved difficult. Here w...

Sympatric speciation illustrates how natural and sexual selection may create new species in isolation without geographic barriers. However, recent genomic reanalyses of classic examples of sympatric speciation reveal complex histories of secondary gene flow from outgroups into the radiation. In contrast, the rich theoretical literature on this proc...

Sexual conflict over the indirect benefits of mate choice may arise when traits in one sex limit the ability of the other sex to freely choose mates but when these coercive traits are not necessarily directly harmful (i.e. forced fertilization per se). While we might hypothesize that females can evolve resistance in order to retain the indirect ben...

According to a recent survey, ecologists and evolutionary biologists feel that theoretical and empirical research should coexist in a tight feedback loop but believe that the two domains actually interact very little. We evaluate this perception using a citation network analysis for two data sets, representing the literature on sexual selection and...

The keystone species concept is used in ecology to describe individual species with disproportionately large effects on their communities. We extend this idea to the level of genes with disproportionately large effects on ecological processes. Such ‘keystone genes’ (KGs) would underlie traits involved in species interactions or causing critical bio...

Sympatric speciation illustrates how natural and sexual selection may create new species in isolation without geographic barriers. However, so far, all genomic reanalyses of classic examples of sympatric speciation indicate secondary gene flow occurred. Thus, there is a need to revisit criteria for demonstrating sympatric speciation in the face of...

Reinforcement is the process whereby assortative mating evolves due to selection against costly hybridization. Sexual imprinting could evolve as a mechanism of reinforcement, decreasing hybridization, or it could potentially increase hybridization in genetically purebred offspring of heterospecific social pairs. We use deterministic population gene...

The evolution of male preferences and of female ornaments in species with traditional sex roles (i.e. polygyny) have been highlighted as areas in need of more active research by an accumulation of recent findings. The theoretical literature on these topics is relatively small and has centered on the evolution of male choice. Mathematical models hav...

Attempts to uncover the genetic basis of female mating preferences and male signals involved in reproductive isolation have discovered intriguing cases in which loci contributing to these traits co-localize in their chromosomal positions. Such discoveries raise the question of whether alleles at certain loci contribute pleiotropically to male and f...

The evolution of mating displays as indicators of male quality has been the subject of extensive theoretical and empirical research for over four decades. Research has also addressed the evolution of female mate choice favoring such indicators. Yet, much debate still exists about whether displays can evolve through the indirect benefits of female m...

Mounting evidence has indicated that engaging in extrapair copulations (EPCs) might be maladaptive or detrimental to females. It is unclear why such nonadaptive female behavior evolves. In this study, we test two hypotheses about the evolution of female EPC behavior using population genetic models. First, we find that both male preference for alloc...

Sexual selection plays several intricate and complex roles in the related processes of local adaptation and speciation. In some cases sexual selection can promote these processes, but in others it can be inhibitory. We present theoretical and empirical evidence supporting these dual effects of sexual selection during local adaptation, allopatric sp...

The large body of theory on speciation with gene flow has brought to light fundamental differences in the effects of two types of mating rules on speciation: preference/trait rules, in which divergence in both (female) preferences and (male) mating traits is necessary for assortment, and matching rules, in which individuals mate with like individua...

In recent years, theoretical models have introduced the concept that ongoing hybridization between “good” species can occur because incomplete reproductive isolation can be a selected optimum. They furthermore show that positive frequency-dependent sexual selection, which is naturally generated by some of the underlying processes that lead to assor...

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 t...

Figure S1. Examples of the evolutionary dynamics under different recombination rates when the internal equilibrium exists. Figure S2. Numerical analysis results of the stabilities of internal equilibria when θ is a constant. Figure S3. Magnified frequency dynamics of the P2 and S2 alleles and linkage disequilibrium (generations ranging from 13,50...

An increasing number of empirical studies in animals have demonstrated male mate choice. However, little is known about the evolution of post-pairing male choice, specifically that which occurs by differential allocation of male parental care in response to female signals. We use a population genetic model to examine whether such post-pairing male...

Mating displays comprise some of the most elaborate traits in animals. A mechanism that can lead to the evolution of such traits is selection through mate choice. Generally, females exhibit stronger mate choice than males, preferentially mating with males that exhibit certain traits. In addition to male displays, the evolution of female mate choice...

Observations of male mate choice are increasingly common, even in species with traditional sex roles. In addition, female traits that bear the hallmarks of secondary sexual characters are increasingly reported. These concurrent empirical trends have led to the repeated inference that, even under polygyny, male mate choice is a mechanism of sexual s...

Speciation in peripheral populations has long been considered one of the most plausible scenarios for speciation with gene flow. In this study, however we identify two additional problems of peripatric speciation, as compared to the parapatric case, that may impede the completion of the speciation process for most parameter regions. First, with (pr...

The unique aspects of speciation and divergence in peripheral populations have long sparked much research. Unidirectional migration, received by some peripheral populations, can hinder the evolution of distinct differences from their founding populations. Here we explore the effects that sexual selection, long hypothesized to drive the divergence o...

Theoretical and empirical research on the evolution of reproductive isolation have both indicated that the effects of sexual selection on speciation with gene flow are quite complex. As part of this special issue on the contributions of women to basic and applied evolutionary biology, I discuss my work on this question in the context of a broader a...

Assortative mating displays and/or preferences can be affected by learning across a wide range of animal taxa, but the specifics of how this learning affects speciation with gene flow are not well understood. We use population genetic models with trait learning to investigate how the identity of the tutor affects the divergence of a self-referent p...

Evolutionary biologists have an array of powerful theoretical techniques that can accurately predict changes in the genetic composition of populations. Changes in gene frequencies and genetic associations between loci can be tracked as they respond to a wide variety of evolutionary forces. However, it is often less clear how to decompose these vari...

Progress in science often begins with verbal hypotheses meant to explain why certain biological phenomena exist. An important purpose of mathematical models in evolutionary research, as in many other fields, is to act as “proof-of-concept” tests of the logic in verbal explanations, paralleling the way in which empirical data are used to test hypoth...

Male ejaculates include large amounts of seminal fluid proteins (Sfps) that influence male sperm competitive success. In spite of their diverse proximate functions, Sfps involved in sperm competition increase male fitness in one of three ways -- 1) "avoidance" proteins help males avoid sperm competition, 2) "defense" proteins help males defend thei...

Significance Sexual selection is generally considered to be an important force in the maintenance of species differentiation. Using population genetic models, we show that when isolated in its purest form of Fisherian sexual selection, sexual selection inhibits rather than assists species maintenance and speciation when isolated populations begin t...

Research on guppies provides the most definitive evidence yet for the rare-male effect — a long-standing hypothesis to explain the perplexing maintenance of variation in traits that are subject to strong mate choice. See Letter p.108

Although learned mate preferences are suspected to have important effects during speciation, theoretical models have largely neglected the effects on speciation and population divergence of within-generational learning, that is, learning based upon prior experience with potential mates. Here, we use population genetic models to address this deficit...

Although sexual selection is an important cause of display evolution, in socially monogamous species (e.g. many birds), displays continue after formation of the pair bond. Here, we consider that these displays evolve because they stimulate the partner to increase investment in offspring. Our study is motivated by elaborate mutual displays in specie...

Inheritance is crucial to the evolutionary process. Although most evolutionary biologists assume that inheritance occurs exclusively through changes in DNA base sequence, it has long been known that inheritance can also occur through epigenetic mechanisms, such as chromatin marking, maternal effects, parasite transmission, or learning. In recent ye...

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The evolution of male mate choice is constrained by costs of choice in species with a male-biased operational sex ratio (OSR). Previous theoretical studies have shown that significant benefits of male choice are required, for example, by mating with more fecund females, in order for these costs to be offset and a male preference to spread. In a ser...

Evidence suggests that female preferences may sometimes arise through sensory bias, and that males may subsequently evolve traits that increase their conspicuousness to females. Here, we ask whether indirect selection, arising through genetic associations (linkage disequilibrium) during the sexual selection that sensory bias imposes, can itself inf...

Learning is widespread in nature, occurring in most animal taxa and in several different ecological contexts and, thus, might play a key role in evolutionary processes. Here, we review the accumulating empirical evidence for the involvement of learning in mate choice and the consequences for sexual selection and reproductive isolation. We distingui...

The extent to which sexual selection is involved in speciation with gene flow remains an open question and the subject of much research. Here, we propose that some insight can be gained from considering the concept of magic traits (i.e., traits involved in both reproductive isolation and ecological divergence). Both magic traits and other, non-magi...

Sexual selection has long been hypothesized to lead to allopatric speciation, and one possible mechanism for this is that its interaction with stochasticity, which perturbs the trait and preference equilibria, can result in different traits being preferred in different populations. Here we specifically examine the role that stochastic changes in se...

Bird song has been hypothesized to play a role in several important aspects of the biology of songbirds, including the generation of taxonomic diversity by speciation; however, the role that song plays in speciation within this group may be dependent upon the ability of populations to maintain population specific songs or calls in the face of gene...

Simulation Equations. (DOC)

In our recent Review in TREE [1], we defined magic traits based on pleiotropy between divergent ecological adaptations and non-random mating. Haller et al. [2] imply doubt in the utility of this definition, concentrating their arguments on effect size (the contribution of a trait to the evolution of reproductive isolation, see [3]). They specifical...

We use birdsong as a case study to ask whether reinforcement can occur via the spread of a genetically determined female preference for a socially inherited (learned) male trait. We envision secondary contact between two neighboring populations with different song dialects. An individual's ability to learn song is confined by a genetic predispositi...

Speciation with gene flow is greatly facilitated when traits subject to divergent selection also contribute to non-random mating. Such traits have been called 'magic traits', which could be interpreted to imply that they are rare, special, or unrealistic. Here, we question this assumption by illustrating that magic traits can be produced by a varie...

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 phenoty...

Population-specific preferences involved in premating isolation may be based on several different types of mating cues. Here, we compare the rates of spread of 12 different mating preferences that reflect preferences for local adaptation, male condition, and reinforcement. We introduce methods to dissect the components of the rate of spread to dete...

The suggestion that speciation may often occur, or be completed, in the presence of gene flow has long been contentious, due to an appreciation of the challenges to maintaining population- or species-specific gene combinations when gene flow is occurring. Linkage disequilibrium between loci involved in postzygotic and premating isolation must often...

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,...

Mate-choice imprinting, the determination of mating preferences at an early age based on an individual's observation of adults, plays a role in mate choice in a wide variety of animals. Theoretical work has thus far been focused either on the effects of mate-choice imprinting on the evolution of the male trait used as a mating cue, or on the evolut...

Male mate selection during polygyny traditionally has been eclipsed in the literature by its female counterpart. Existing models that have studied male mate choice have concluded that males with genetically inherited preferences for females exhibiting particular traits are often less fit than males without such a preference, leading to preference l...

One hypothesis explaining the species richness of the songbirds is based on the fact that these species generally acquire their songs socially rather than genetically. Here we consider the outcome of secondary contact between birds that have developed distinct song dialects in allopatry. We ask 2 questions: 1) given a fixed probability of learning,...

Male mate choice, expressed through courtship preferences, sometime occurs even under the mating system of polygyny, when the operational sex ratio is skewed toward males. The conditions under which male mate choice may be expected during polygyny are not well established. Servedio and Lande (2006, Evolution 60:674-685), assuming strict polygyny wh...

Male color polymorphism may be an important precursor to sympatric speciation by sexual selection, but the processes maintaining such polymorphisms are not well understood. Here, we develop a formal model of the hypothesis that male color polymorphisms may be maintained by variation in the sensory environment resulting in microhabitat-specific sele...

Interbreeding between species (hybridization) typically produces unfit offspring. Reduced hybridization should therefore be favored by natural selection. However, this is difficult to accomplish because hybridization also sets the stage for genetic recombination to dissociate species-specific traits from the preferences for them. Here we show that...

Conspecific gamete precedence, the usage of conspecific sperm by a female that mates with both a conspecific and a heterospecific male, has been found in many taxa. We construct a population genetic model to examine the evolution of conspecific gamete precedence and its coevolution with premating isolation in the process of reinforcement. Our findi...

Evidence has been accumulating to support the process of reinforcement as a potential mechanism in speciation. In many species, mate choice decisions are influenced by cultural factors, including learned mating preferences (sexual imprinting) or learned mate attraction signals (e.g., bird song). It has been postulated that learning can have a stron...

Hosts either tolerate avian brood parasitism or reject it by ejecting parasitic eggs, as seen in most rejecter hosts of common cuckoos, Cuculus canorus, or by abandoning parasitized clutches, as seen in most rejecter hosts of brown-headed cowbirds, Molothrus ater. What explains consistent variation between alternative rejection behaviours of hosts...

Examples of male mate choice are becoming increasingly common, even in polygynous species. We create a series of population genetic models to examine the evolutionary equilibria and dynamics resulting from male mate choice during polygyny, alone and in the context of mutual mate choice by both sexes. We find that unless males with a preference are...

Many models have investigated how the process of speciation may occur in sympatry. In these models, individuals are either asexual or mate choice is determined by very simple rules. Females, for example, may be assumed either to compare their phenotype to that of a potential mate, preferring to mate with similar males (phenotype matching), or to po...