A comprehensive overview of the developmental basis and adaptive significance of a textbook polymorphism: head asymmetry in the cichlid fish Perissodus microlepis

Abstract

Identifying the evolutionary and developmental bases of adaptive phenotypes is of central interest in evolutionary biology. Cichlid fishes have been a useful research model due to their extraordinary phenotypic diversity reflecting adaptations to often very narrow niches. Among them, the scale-eating Perissodus microlepis is considered to be a textbook example for balanced polymorphism: its asymmetric head and handed behavior is thought to be maintained by negative frequency-dependent selection via prey-predator interactions. However, several contradictory findings and open questions have emerged in recent years, challenging our understanding of this model. Here, we review existing evidence for both genetic and non-genetic effects influencing head asymmetry, the association between morphological asymmetry and behavioral laterality, and the identification of signatures of balancing selection. Recent technological and theoretical developments have opened new exciting research avenues that can help identifying the drivers of adaptive traits in P. microlepis and other nonmodel organisms, and we discuss promising directions worth exploring. We highlight the importance of using integrative approaches that analyze genetic, environmental, and epigenetic variation in natural populations to aid a comprehensive understanding of why cichlids are so diverse and how Hydrobiologia (2019) 832:65-84 https://doi.org/10.1007/s10750-018-3800-z( 0123456789().,-volV) (0123456789().,-volV) evolution has produced and continues to generate such a vibrant and often complex phenotypic diversity.

Surprising spatiotemporal stability of a multi-peak fitness landscape revealed by independent field experiments measuring hybrid fitness

“…The rare evolution, high performance demands, and low caloric payoffs of scale‐eating suggest that a wide and deep fitness valley may isolate this niche from all other ecological niches. First, scale‐eating (lepidophagy) is a particularly rare trophic niche among fishes and has evolved independently only 19 times across diverse marine, coastal, riverine, and lacustrine environments (Sazima 1983; Martin and Wainwright 2013c; Kolmann et al 2018; St John et al 2019; Grubh and Winemiller 2004; Janovetz 2005; Koblmüller et al 2007; Raffini and Meyer 2018; Hori 1993). Scale‐eating only evolved once in Cyprinodontiformes and is separated by 168 million years of evolutionary time from the most closely related African cichlid scale‐eating specialists, providing a quantitative measure of the ecological novelty of this niche (Martin and Wainwright 2013c).…”

Structural manipulations of a shelter resource reveal underlying preference functions in a shell-dwelling cichlid fish

“…Alternatively, the use of right-coiled shells over evolutionary time may have generated a lateralised behavioural response in shell-dwelling cichlids. Behavioural, morphological, and even neuroanatomical lateralisation are well-known in the scale-eating Tanganyikan cichlid Perissodus microlepis [34][35][36][37] and with our technique the possibility to explore lateralised behaviour and morphology more broadly in shell-dwelling cichlids offers an exciting new avenue of research in this area.…”

Habitat degradation and predators have independent trait-mediated effects on prey

“…The presence of strongly selective predation 52 , and the phenotypic plasticity displayed by juvenile fishes generally (e.g. 53,54 ), suggests that the benefits of developing a larger relative false eyespot outweighs the costs of having a smaller true eye, though field test will be needed to support this assertion.…”