Abstract

The scale‐eating cichlid fish Perissodus microlepis is a textbook example of bilateral asymmetry due to its left or right‐bending heads and of negative frequency‐dependent selection, which is proposed to maintain this stable polymorphism. The mechanisms that underlie this asymmetry remain elusive. Several studies had initially postulated a simple genetic basis for this trait, but this explanation has been questioned, particularly by reports observing a unimodal distribution of mouth shapes. We hypothesize that this unimodal distribution might be due to a combination of genetic and phenotypically plastic components. Here, we expanded on previous work by investigating a formerly identified candidate SNP associated to mouth laterality, documenting inter‐individual variation in feeding preference using stable isotope analyses, and testing their association with mouth asymmetry. Our results suggest that this polymorphism is influenced by both a polygenic basis and inter‐individual non‐genetic variation, possibly due to feeding experience, individual specialization, and intraspecific competition. We introduce a hypothesis potentially explaining the simultaneous maintenance of left, right, asymmetric and symmetric mouth phenotypes due to the interaction between diverse eco‐evolutionary dynamics including niche construction and balancing selection. Future studies will have to further tease apart the relative contribution of genetic and environmental factors and their interactions in an integrated fashion.

Highlights

  • To verify a previously identified SNP and its relationship with the degree of mouth asymmetry, we explored the association between the candidate SNP 56537-113 and mouth bending angle. 168 samples were successfully genotyped at this locus (Table S2)

  • The results confirm that the candidate SNP 56537-113 is associated with mouth bending angle, which explains a relatively small amount (6%) of phenotypic variation, and provide further support for the hypothesis that head asymmetry in P. microlepis has a complex genetic basis

  • We introduce a comprehensive hypothesis potentially explaining how these genetic and non-genetic cues jointly influence the direction and the degree of mouth asymmetry as well as the maintenance of intraspecific variation

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Summary

Introduction

Stable polymorphisms such as conspicuous asymmetry (departure from symmetry in morphology) or handedness (lateralized behavior) have repeatedly emerged in both vertebrates and invertebrates (Ludwig, 1932; Palmer, 2004, 2009, 2016; e.g., Hori, 1993; Kurvers et al, 2017; Lucky, Ihara, Yamaoka, & Hori, 2012; Matsui, Takeuchi,& Hori, 2013; Takeuchi & Hori, 2008; Tobo, Takeuchi, & Hori, 2012). While previous studies investigated genomic loci underlying the difference between L and R morphs (i.e., the direction of mouth asymmetry, Hori, 1993; Hori et al, 2007; Lee et al, 2015; Palmer, 2010; Raffini et al, 2017; Stewart & Albertson, 2010), here, for the first time we extend this work by analyzing the association between the candidate locus and mouth bending angle, a more precise and continuous quantification of asymmetry

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