Ecology Letters, (2011) doi: 10.1111/j.1461-0248.2011.01606.x REVIEW AND SYNTHESIS Ecology, sexual selection and speciation Abstract Martine E. Maan* and Ole The spectacular diversity in sexually selected traits among animal taxa has inspired the hypothesis that divergent Seehausen sexual selection can drive speciation. Unfortunately, speciation biologists often consider sexual selection in Institute of Ecology and Evolution, isolation from natural selection, even though sexually selected traits evolve in an ecological context: both University of Bern, Baltzerstrasse 6, preferences and traits are often subject to natural selection. Conversely, while behavioural ecologists may CH-3012 Bern, Switzerland; and address ecological effects on sexual communication, they rarely measure the consequences for population Eawag Centre of Ecology, Evolution divergence. Herein, we review the empirical literature addressing the mechanisms by which natural selection and Biogeochemistry (CEEB), and sexual selection can interact during speciation. We find that convincing evidence for any of these scenarios Seestrasse 79, CH-6047 is thin. However, the available data strongly support various diversifying effects that emerge from inter- Kastanienbaum, Switzerland actions between sexual selection and environmental heterogeneity. We suggest that evaluating the evolu- *Correspondence: E-mail: tionary consequences of these effects requires a better integration of behavioural, ecological and evolutionary [email protected] research. Keywords Adaptation, assortative mating, divergence, environmental heterogeneity, good genes, magic trait, mate choice, natural selection, pleiotropy, reinforcement. Ecology Letters (2011) the sexual ornament in terms of mating success are exactly matched by INTRODUCTION disadvantages in terms of survival. Spatial environmental variation in The past two decades have yielded empirical support for the the costs of display can generate between-population variation in hypothesis that divergent selection can drive speciation (Schluter equilibrium values of trait and preference. Additional selective forces 2009; Sobel et al. 2010). For example, divergent ecological adaptation may interact with Fisherian coevolution. In particular, mate preferences can reduce the spatial or temporal coincidence of mating, sexual traits are often subject to natural selection, for example when choosiness and preferences can diverge as a by-product of ecological adaptation, entails predation risk or when environmental conditions affect signal or assortative mating may evolve as a result of selection favouring perception. Moreover, mate preferences may target display traits that ecological specialists. At the same time, divergent sexual selection may co-vary with ecological performance, such as parasite resistance or cause speciation – an insight that Coyne & Orr (2004) considered one foraging ability. These interactions provide several mechanisms by of the most important findings in recent speciation research, although which environmental heterogeneity can affect both mating preferences the evidence is mostly comparative (Ritchie 2007). and sexually selected traits, potentially contributing to population As organisms are subject to both natural and sexual selection divergence and speciation. simultaneously, important open questions concern how these interact Here, we review the empirical support for the mechanisms by which during speciation, and whether such interactions tend to facilitate or natural and sexual selection may interact during speciation, and we ask rather constrain speciation. Intuitively, one may expect that species if their interaction tends to facilitate or rather constrain speciation. We characterised by strong sexual selection are more likely to evolve pre- focus on intersexual selection in animals and we do not consider mating isolation. This is because sexual selection directly affects mating sexual conflict, because very little is known about potential interac- patterns and the emergence of linkage disequilibrium (Kirkpatrick & tions with ecology (Fricke et al. 2009). Ravigne´ 2002), and because sexually selected species often express secondary sexual traits and mating preferences that could be recruited THEORETICAL CONCEPTS by selection for assortative mating. Moreover, sexually selected traits evolve rapidly and often differ markedly between closely related taxa, To facilitate detection of interactions between natural and sexual and comparative studies indicate that sexually selected taxa may be selection, and to evaluate whether they promote or constrain more species-rich (reviewed in Kraaijeveld et al. 2010). speciation, we briefly discuss a few definitions and distinctions. Some The null model of sexual selection is the Fisher process (Prum 2010), of these are subject to inconsistent usage and recurrent confusion. whereby preferences and traits become genetically correlated, allowing them to coevolve and sometimes Ôrun awayÕ to extreme values. Such Assortative mating and sexual selection coevolution may proceed independently from ecological conditions. However, sexual selection will often be modified or opposed by Assortative mating does not automatically imply sexual selection. ecological selection. For example, natural selection may impose a cost Sexual selection emerges from competition and mate choice that on sexual display, causing the rapid coevolution towards more extreme generate variation in mating success among individuals of the same preferences and traits to reach equilibrium where the advantages of sex. If this variation is mediated by heritable traits, sexual selection Ó 2011 Blackwell Publishing Ltd/CNRS 2 M. E. Maan and O. Seehausen Review and Synthesis Table 1 Non-random mating driven by natural selection: mechanisms and hypothetical scenarios Mechanism of non-random mating Link between natural selection and mate choice Pleiotropy:(ÔmagicÕ) trait under divergent Direct selection: mate choice divergence Indirect selection: mate choice natural selection also controls favoured by direct selection divergence favoured by selection non-random mating for offspring fitness One-allele: the same Similarity Divergent ecological selection on Spread of size-assortative mating Spread of size-assortative mating mating trait spreads body size in a population with driven by higher fertilisation rate in driven by selection against in two diverging size-assortative mating size-matched pairs, in a population intermediates, in a population populations experiencing divergent selection on experiencing divergent selection body size on body size Preference-trait Preferences diverge following divergent Sexual selection for ecological Sexual selection for ecological ecological selection on morphology, because performance becomes divergent performance becomes divergent of female imprinting on father’s morphology between alternative ecological between alternative ecological (independent of own morphology) regimes – e.g. driven by selection for regimes – e.g. driven by selection paternal provisioning on offspring fitness Two-allele: two different Similarity Impossible? One subpopulation evolves One subpopulation evolves mating traits spread size-assortative mating because size-assortative mating because in two diverging size-matched matings have higher of selection against intermediate populations fertilisation rate there; another sizes; another subpopulation subpopulation evolves evolves colour-assortative mating colour-assortative mating because because of selection against colour-matched matings have lower intermediate colours, in a predation rate there, in a population population experiencing experiencing divergent ecological divergent ecological selection selection on colour and size on colour and size Preference-trait Infection with habitat-specific Male ornaments are habitat-specific Male ornaments are parasites changes female sensory indicators of parasite resistance; habitat-specific indicators of abilities, which pleiotropically affect preference divergence is driven by parasite resistance; preference preferences for male ornamentation infection avoidance during mating divergence is driven by selection for resistant offspring (reinforcement-like) affects the frequency of trait values and the underlying alleles in a two-allele scenario, different alleles spread in each population, such as population. In contrast, assortative mating may only reorganise alleles for different habitat or mating preferences. In theory, one-allele variation by changing genotype frequencies without affecting allele mechanisms are more conducive to speciation than two-allele frequencies. Theoretical models and simulation studies of sympatric mechanisms, particularly when geographical isolation is incomplete, and parapatric speciation consider a variety of scenarios in this regard. because recombination cannot break the linkage disequilibrium Some analytical models (Kondrashov & Shpak 1998; Kirkpatrick & between trait and preference. However, distinguishing them in natural Ravigne´ 2002) are explicit about including just assortative mating. In systems can be difficult, as both mechanisms may operate simulta- simulation studies this can be more difficult to see. Some apply a neously or at different stages of divergence (see e.g. Servedio 2008). normalisation procedure such that all phenotypes obtain equal mating Moreover, the paradigm is sometimes confused with the distinction success (e.g. Dieckmann & Doebeli 1999), while others allow selection between