Mechanisms of Assortative Mating in Speciation with Gene Flow: Connecting Theory and Empirical Research (original) (raw)

Geography, assortative mating, and the effects of sexual selection on speciation with gene flow

Evolutionary Applications, 2015

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 assessment of the patterns of sexual selection that lead to, versus inhibit, the speciation process, as derived from theoretical research. In particular, I focus on how two factors, the geographic context of speciation and the mechanism leading to assortative mating, interact to alter the effect that sexual selection through mate choice has on speciation. I concentrate on two geographic contexts: sympatry and secondary contact between two geographically separated populations that are exchanging migrants and two mechanisms of assortative mating: phenotype matching and separate preferences and traits. I show that both of these factors must be considered for the effects of sexual selection on speciation to be inferred.

Effects of genetic architecture on the evolution of assortative mating under

2011

We consider a model of sympatric speciation due to frequency-dependent competition, in which it was previously assumed that the evolving traits have a very simple genetic architecture. In the present study, we numerically analyze the consequences of relaxing this assumption. First, previous models assumed that assortative mating evolves in infinitesimal steps. Here, we show that the range of parameters for which speciation is possible increases when mutational steps are large. Second, it was assumed that the trait under frequency-dependent selection is determined by a single locus with two alleles and additive effects. As a consequence, the resultant intermediate phenotype is always heterozygous and can never breed true. To relax this assumption, here we add a second locus influencing the trait. We find three new possible evolutionary outcomes: evolution of three reproductively isolated species, a monomorphic equilibrium with only the intermediate phenotype, and a randomly mating population with a steep unimodal distribution of phenotypes. Both extensions of the original model thus increase the likelihood of competitive speciation.

Frequency-Dependent Selection and the Evolution of Assortative Mating

Genetics, 2008

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 non-equilibrium 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.

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

Proceedings of The Royal Society B: Biological Sciences, 2010

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.

Emergence and loss of assortative mating in sympatric speciation

Journal of Theoretical Biology, 2009

We have studied an agent model which presents the emergence of sexual barriers through the onset of assortative mating, a condition that might lead to sympatric speciation. In the model, individuals are characterized by two traits, each determined by a single locus A or B. Heterozygotes on A are penalized by introducing an adaptive difference from homozygotes. Two niches are available. Each A homozygote is adapted to one of the niches. The second trait, called the marker trait has no bearing on the fitness. The model includes mating preferences, which are inherited from the mother and subject to random variations. A parameter controlling recombination probabilities of the two loci is also introduced. We study the phase diagram by means of simulations, in the space of parameters (adaptive difference, carrying capacity, recombination probability). Three phases are found, characterized by (i) assortative mating, (ii) extinction of one of the A alleles and (iii) Hardy-Weinberg like equilibrium. We also make perturbations of these phases to see how robust they are. Assortative mating can be gained or lost with changes that present hysteresis loops, showing the resulting equilibrium to have partial memory of the initial state and that the process of going from a polymorphic panmictic phase to a phase where assortative mating acts as sexual barrier can be described as a first-order transition.

Sexual selection and magic traits in speciation with gene flow

Current Zoology, 2012

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-magic”, traits can contribute to speciation via a number of specific mechanisms. We argue that many of these mechanisms are likely to differ widely in the extent to which they involve sexual selection. Furthermore, in some cases where sexual selection is present, it may be prone to inhibit rather than drive speciation. Finally, there are a priori reasons to believe that certain categories of traits are much more effective than others in driving speciation. The combination of these points suggests a classification of traits that may shed light on the broader role of sexual selection in speciation with gene flow. In particular, we suggest that ...

The role of mate-choice copying in speciation and hybridization

Biological Reviews, 2018

Mate-choice copying, a non-genetic mechanism of mate choice, occurs when an individual (typically a female) copies the mate choice of other individuals via a process of social learning. Over the past 20 years, MCC has consistently been shown to affect mate choice in several species, by modifying genetically-based mating preferences. This behaviour has been claimed by several authors to have a significant role in evolution. Because it can cause or increase skews in male mating success, it seems to have the potential to induce a rapid change of the directionality and rate of sexual selection, possibly leading to divergent evolution and speciation. Theoretical work has, however, been challenging this view, showing that copying may decelerate sexual selection and that linkage disequilibrium cannot be established between the copied preference and the male trait, because females copy from unrelated individuals in the population, making an invasion of new and potentially fitter male traits difficult. Given this controversy, it is timely to ask about the real impact of mate-choice copying on speciation. We propose that a solution to this impasse may be the existence of some degree of habitat selection, which would create spatial structure, causing scenarios of micro-allopatry, overcoming the problem of the lack of linkage disequilibrium. As far as we are aware, the potential role of mate choice copying on fostering speciation in micro-allopatry has not been tackled. Also important is that the role of mate-choice copying has generally been discussed as being a barrier to gene flow. However, as we see it, mate-choice copying may actually play a key role in facilitating gene flow, thereby fostering hybridization. Yet, the role of mate-choice copying on hybridization has so far been overlooked, although the conditions under which it might occur are much more likely, or less stringent, than those favouring speciation. Hence, a conceptual framework is needed to identify the exact mechanisms and the conditions under which speciation or hybridization are expected. Here, we develop such a framework to be used as a roadmap to future research at the intersection of these research areas.

The counterintuitive role of sexual selection in species maintenance and speciation

Proceedings of the National Academy of Sciences, 2014

The pronounced and elaborate displays that often differ between closely related animal species have led to the common assumption that sexual selection is important in speciation, especially in geographically separated populations. We use population genetic models to examine the ability of Fisherian sexual selection to contribute to lasting species differentiation by isolating its effect after the onset of gene flow between allopatric populations. We show that when sexually selected traits are under ecologically divergent selection, the situation most favorable to speciation, mating preferences tend to introgress faster than trait alleles, causing sexual selection to counter the effects of local adaptation. As a consequence, the net amount of trait divergence often drops with stronger Fisherian sexual selection. Furthermore, alleles for progressively weaker preferences spread in this context until sexual selection is removed. The effects of pure Fisherian sexual selection on species maintenance are thus much more inhibitory than previously assumed.

Sexual selection and the detection of ecological speciation

2006

Context: Ecological speciation is commonly inferred with evidence of the parallel evolution of pre-mating isolation: individuals from populations in similar environments show higher mating success in laboratory experiments than do individuals from different environments. Critically, this should hold even for mating crosses among populations that are from different locations that represent independent evolutionary lineages.