Abstract

Natural color polymorphisms are widespread across animal species and usually have a simple genetic basis. This makes them an ideal system to study the evolutionary mechanisms responsible for maintaining biodiversity. In some populations of the intertidal snail Littorina fabalis, variation in shell color has remained stable for years, but the mechanisms responsible are unknown. Previous studies suggest that this stability could be caused by frequency-dependent sexual selection, but this hypothesis has not been tested. We analyzed shell color polymorphism in mating pairs and surrounding unmated individuals in two different populations of L. fabalis to estimate sexual fitness for color, as well as assortative mating. The estimated effective population size from neutral markers allowed us to disregard genetic drift as the main source of color frequency changes across generations. Shell color frequency was significantly correlated with sexual fitness showing a pattern of negative frequency dependent selection with high disassortative mating for color. The results suggested a contribution of male mate choice to maintain the polymorphism. Finally, the implementation of a multi-model inference approach based on information theory allowed us to test for the relative contribution of mate choice and mate competition to explain the maintenance of color polymorphism in this snail species.

Highlights

  • Negative frequency-dependent selection (NFDS) operates when the relative fitness of a morph within a natural population is an inverse function of its relative frequency, i.e., the more abundant a morph is, the lower its fitness (Wright, 1939)

  • Shell color polymorphism in L. fabalis is persistent despite expected strong genetic drift

  • We have otherwise found that color polymorphism in this species follows a NFDS pattern when studying the sexual component of fitness

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Summary

Introduction

Negative frequency-dependent selection (NFDS) operates when the relative fitness of a morph within a natural population is an inverse function of its relative frequency, i.e., the more abundant a morph is, the lower its fitness (Wright, 1939). Patterns of NFDS can arise in several distinct, non-exclusive scenarios: driven by predation (apostatic selection), where less frequent morphs have a survival advantage (Tucker, 1991; Olendorf et al, 2006; Fitzpatrick et al, 2009; Weir, 2018); by sexual conflict, where less frequent morphs of one sex obtain fitness benefits in detriment or against fitness interests in the other sex (Svensson et al, 2005; Gosden and Svensson, 2007); by mate competition, where the less frequent morph within one sex obtains a greater number of matings than the common one when competing for them (Sinervo and Lively, 1996; Bleay et al, 2007; Rios-Cardenas et al, 2018); and by mate choice, in cases when rare or dissimilar morphs are preferred and have relatively more matings (Hughes et al, 2013; Chouteau et al, 2017; Valvo et al, 2019). We refer to these two scenarios as sexual fitness (following Hedrick, 1983, p.163; Bell, 2008, p.167), a component of fitness defined by the capacity of individuals to find mates

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