Evolutionary Applications Evolutionary Applications ISSN 1752-4571 REVIEW AND SYNTHESES Geography, assortative mating, and the effects of sexual selection on speciation with gene flow Maria R. Servedio Department of Biology, University of North Carolina, Chapel Hill, NC, USA Keywords Abstract allopatry, assortative mating, migration, secondary contact, sympatry, two-island Theoretical and empirical research on the evolution of reproductive isolation model. 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 Correspondence women to basic and applied evolutionary biology, I discuss my work on this Maria R. Servedio, Department of Biology, question in the context of a broader assessment of the patterns of sexual selection University of North Carolina, CB# 3280, Coker that lead to, versus inhibit, the speciation process, as derived from theoretical Hall, Chapel Hill, NC 27599, USA. Tel.: +1-919-8432692; research. In particular, I focus on how two factors, the geographic context of spe- fax: +1-919-9621625; ciation and the mechanism leading to assortative mating, interact to alter the e-mail: [email protected] effect that sexual selection through mate choice has on speciation. I concentrate on two geographic contexts: sympatry and secondary contact between two geo- Received: 28 February 2015 graphically separated populations that are exchanging migrants and two mecha- Accepted: 1 July 2015 nisms of assortative mating: phenotype matching and separate preferences and traits. I show that both of these factors must be considered for the effects of sex- doi:10.1111/eva.12296 ual selection on speciation to be inferred. 2004; selection against hybrids can fall into this category, Introduction e.g., Dobzhansky 1937; Muller 1942). To understand when The fascination that biologists have long had with specia- speciation may occur in the face of gene flow, one must tion has increased in recent decades as we have gained a understand the joint action of both of these processes. better and better understanding of the complexity of this Assortative mating and divergent selection are, however, engine of biodiversity. One of the most intriguing aspects not necessarily completely independent components of the of speciation is how it might proceed under the most diffi- speciation process. The mechanisms that generate assorta- cult of circumstances, namely in the face of gene flow. Gene tive mating, in almost all cases (except, e.g., symmetric flow poses an especially interesting problem for evolution- grouping models, Norvaisas and Kisdi 2012), generate dif- ary theorists because it counters the forces driving differen- ferential mating success among genotypes, that is, sexual tiation between species, leading to continued cohesion selection. To understand the importance of this, first it is across them. The problem of speciation with gene flow also critical to keep in mind that sexual selection can be a has conservation implications; the onset of gene flow after potent evolutionary force, in fact one that is often more a period of allopatric divergence can erode differences powerful than viability selection (e.g., Hoekstra et al. 2001; between species or races, posing important questions Kingsolver et al. 2001). Just as sexual selection may drive regarding how species differences can be maintained, or the evolution of traits within a population, it has the poten- how speciation may continue to proceed. tial to lead to differences between species and has often Speciation in the presence of gene flow, in sexual species, been speculated to be an important factor in the speciation can be driven by two general processes: (i) nonrandom process, especially in allopatry (West-Eberhard 1983; Pan- mating that results in assortative mating, the mating of like huis et al. 2001; Ritchie 2007). The role of sexual selection with like, which reduces gene flow between groups, and (ii) in speciation with gene flow, however, is less clear; some divergent selection, which favors extremes in a population studies suggest it can drive the speciation process, while and thus can lead to a splitting of the species (e.g., Kirk- others suggest it can inhibit it, under different conditions patrick and Ravigne 2002; Coyne and Orr 2004; Gavrilets (e.g., Bolnick and Fitzpatrick 2007; Mallet 2008; Nosil © 2015 The Author. Evolutionary Applications published by John Wiley & Sons Ltd. This is an open access article under the terms of the Creative 91 Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. Geography, assortative mating and speciation Servedio 2008; Maan and Seehausen 2011; Smadja and Butlin 2011; can potentially lead to speciation if it is directional, in Servedio and Kopp 2012). opposite directions in each population (Fig. 1A, middle, In this paper, I maintain that to understand the role that orange arrows). In other words, this opposing directional sexual selection plays in speciation with gene flow, it is crit- selection within each population approximates divergent ical to consider two key factors. First, the geographic con- selection when both populations are considered together. text in which gene flow occurs can be very important, as it Similarly, selection within each population could poten- can alter the patterns of selection that lead to divergence. tially be stabilizing, but for different optima (Fig. 1A, mid- Second, there are two fundamentally different mechanisms dle, green arrows). Several theoretical studies have by which assortative mating can occur, even when only considered ecological speciation between two populations considering those forms of assortative mating that act exchanging migrants using ‘two-island’ models with these through mate choice (as I do here): phenotype matching types of selection regimes (often including intrinsic selec- and separate preferences and traits. These two mechanisms tion against hybrids as an additional force favoring diver- generate sexual selection in different ways. As part of this gence, e.g., Felsenstein 1981; Liou and Price 1994; Servedio special issue on the contributions of women to basic and and Kirkpatrick 1997; Proulx and Servedio 2009). On the applied evolutionary biology, I will review theoretical other hand, sympatric speciation, which occurs within a research addressing how the geography of speciation and single population, requires that selection be divergent per se type of assortative mating interact to affect the role of sex- (Fig. 1B, middle). This selection pattern can emerge either ual selection in speciation with gene flow, with an emphasis as a result of disruptive selection resulting from, for exam- on synthesizing my own views and contributions to our ple, bimodally distributed resources, or even because of understanding of this problem, particularly in the case of competition among individuals when resources are uni- secondary contact. modal (e.g. Dieckmann and Doebeli 1999; Burger€ et al. 2006; Pennings et al. 2008). The differences in the mode of selection required with Geography and speciation with gene flow and without geographic separation are important, because The geographic background upon which the process of spe- ciation proceeds has long been considered the primary determinant of the ease of speciation, but in recent years, (A)Geographic separation (B) there has been a growing recognition that geographic clas- Sympatry sifications capture only part of the picture (Butlin et al. 2008; Fitzpatrick et al. 2009; Marie Curie Speciation Net- Geography work 2012). In a simplistic view, the key distinction between the geographic categories of allopatric, parapatric, and sympatric speciation can be thought of as whether gene Population 1 flow between incipient species is possible; allopatric specia- tion occurs in the absence of gene flow, while parapatric and sympatric speciation assume the occurrence of varying degrees of gene flow (Mayr 1963). We now understand that Selection pattern there are finer geographic distinctions that can have impor- Population 2 phenotype tant effects on the likelihood of speciation (see Coyne and Orr 2004; Fitzpatrick et al. 2009). Furthermore, even within cases of speciation with gene flow, the geographic phenotype context can affect patterns of gene flow, which can ulti- Directional (opposite directions) mately have important effects on the likelihood of diver- Divergent Stabilizing (different optima) gence (Servedio and Kirkpatrick 1997; Gavrilets 2004; Kisdi Selection mode and Prikopil 2011; Rettelbach et al. 2013). As mentioned in the Introduction, one of the essential Figure 1 Schematic of the modes of selection necessary to drive speci- components of speciation with gene flow is divergent selec- ation with gene flow in the scenarios of (A) allopatric populations that tion. Selection must be divergent, that is, between the are exchanging migrants and (B) sympatric speciation. The pictures associated with the labels for ‘geography’ show discrete traits for the incipient species. If the diverging pair of populations is, purpose of illustration, but these scenarios are also relevant for quanti- however, geographically separated but undergoing gene tative traits, as shown under ‘selection pattern’. The populations in (A) flow through the exchange of migrants (Fig. 1A, top, note are drawn as if they have already diverged to some extent. The arrows that I still refer to these as ‘allopatric’