Mate Choice Contributes to the Maintenance of Shell Color Polymorphism in a Marine Snail via Frequency-Dependent Sexual Selection

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.

Negative assortative mating and maintenance of shell colour polymorphism in Littorina (Neritrema) species

“…Besides speciation being the main focus of the evolutionary research carried out in these species (e.g. Morales Although there are alternative explanations (see Taborsky et al 2009), assortative mating in simple organisms such as marine gastropods is presumably caused by mate choice (Ng et al 2019;Estévez et al 2020). On the other hand, negative assortative mating is directly related to negative-frequency dependent selection, as it has been shown both theoretically (Pusey and Wolf 1996;Hedrick et al 2016 and and empirically in several species (Takashi and Hori 2008;Field and Barrett 2012;Holman et al 2013;Hedrick et al 2016 andEstévez et al 2020).…”

Negative frequency‐dependent selection maintains shell banding polymorphisms in two marine snails (Littorina fabalis and Littorina saxatilis)

“…Otherwise, we can say that sexual selection is not contributing to the maintenance of the band polymorphism. The way data were obtained for L. fabalis inEstévez et al (2020) allowed us to estimate this component of natural selection, and we found nor a pattern of NFDS using sexual fitness (females: F 1,7 = 0.53, p =0.497| males: F 1,7 = 0.66, p = 0.452) nor…”

“…Mating pairs and unmated individuals of L. fabalis were collected from the Fucus spp. canopy in a rocky shore located in Abelleira, A Coruña, NW Spain (42°48′0.30″N-9°1′14.87″W), for a period of 7 years from 2011 to 2017 (see further details in Estévez et al, 2020). The density of the population is relatively large compared with other populations, with tens of individuals per algae.…”

“…The effective population size (N e ) obtained by Estévez et al (2020) was used here to test whether changes in allele frequencies for the polymorphism of bands in L. fabalis could be explained by genetic drift. The genotypes of the microsatellites analyzed in this study were used to estimate the N e using the linkage disequilibrium method as implemented in the software NeEstimator v.2.01 (Do et al, 2014).…”

“…The data for this study were obtained from two independent research efforts. For L. fabalis, phenotypic data on banding frequency were obtained from a study on shell color and mate choice (Estévez et al, 2020), although the data on banding are presented here for the first time. For L. saxatilis, we used published data from a study by Johannesson and Butlin (2017; https://doi.org/10.5061/ dryad.427p0).…”