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

Abstract

Colour polymorphism is a widespread phenomenon in natural populations of several species. In particular, it is especially common on marine gastropod species from the genus Littorina. Recently, it has been argued that intrapopulation shell colour polymorphism in Littorina fabalis could be caused by negative frequency-dependent sexual selection via a mechanism of mate choice (indirectly estimated via negative assortative mating). Here we try to determine the existence of negative assortative mating in three species of the subgenus Neritrema (L. fabalis, L. obtusata, L. saxatilis) that share a similar shell colour polymorphism, in order to ascertain if this mechanism could represent an ancestral character in this subgenus that could be contributing to the maintenance of the colour polymorphism in each species.Here, we collected or reanalysed from previous studies a sample of mating pairs of the three species from seven locations from NW Spain and NE Russia and estimated assortative mating using the I PSI index. Our results show that all species and populations show a systematic tendency towards negative assortative mating when shell colour is grouped in the broad categories: 'light' and 'dark'. Although, a more detailed analysis of each colour individually suggests that shell colour may not be the main target of assortative mating, but perhaps physically linked to another trait or through pleiotropic effects. This hypothesis opens interesting new lines of research in Littorina snails.

Shell color polymorphism in marine gastropods

“…L . saxatilis shows shell color variation within several populations of the Galician coasts (NW Spain), including orange, white and banded color morphs (Fischer‐Piette & Gaillard, 1961 ; Fischer‐Piette et al, 1961 ; Gefaell et al, 2021 ; Sacchi, 1979 ; Torelli, 1983 ). Northern populations of L .…”

“…NFDS can also be driven by sexual selection, and among these scenarios, we find sexual conflict (Gosden & Svensson, 2007 ; Svensson et al, 2005 ), mate competition (Rios‐Cardenas et al, 2018 ; Sinervo & Lively, 1996 ), and mate choice (Takashi & Hori, 2008 ). However, in organisms with a limited behavioral repertoire, such as most marine gastropods, only mate choice has been linked to NFDS for shell color (Estévez et al, 2020 ; Gefaell et al, 2021 ; Rolán‐Alvarez & Caballero, 2000 ; Rolán‐Alvarez & Ekendahl, 1996 ; Rolán‐Alvarez et al, 2012 , 2015b ).…”

“…In the genus Littorina , negative assortative mating has been used as an indirect proxy for mate‐choice‐driven NFDS (see Gefaell et al, 2021 and references therein). Rolán‐Alvarez et al ( 2012 , 2015b ) collected mated and unmated individuals of L .…”

“…obtusata and L . saxatilis , suggesting that male mate choice may be an ancestral behavioral trait driving NFDS on shell color, and thereby promoting polymorphism in at least certain populations of these species (Gefaell et al, 2021 ). However, since the relationship between negative assortative mating, mate choice and NFDS is not straightforward and direct, experimental confirmations of this link must be made before the mate choice‐driven NFDS hypothesis is considered definitively corroborated.…”

“…Estévez et al ( 2020 ), as well as Gefaell et al ( 2021 ), have suggested the possibility that in the abovementioned cases of negative assortative mating and mate choice for shell color in several species of the genus Littorina , the real target of (sexual) selection may not be the color itself, but another genetically correlated trait, tightly linked to it. An argument in favor of this hypothesis, in addition to the observed mating patterns in different Littorina populations (see Gefaell et al, 2021 ), is that it is highly unlikely that marine gastropods can see colors, a prerequisite for mate choice based on shell color. This has led to the hypothesis that littorinids can somehow recognize the different shell colors without any visual cue, or alternatively each of these colors may be associated with some other trait crucial to biological fitness.…”