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Exploring the origin and maintenance of biodiversity : insights from the bilaterally asymmetrical cichlid fish Perissodus microlepis

Exploring the origin and maintenance of biodiversity : insights from the bilaterally asymmetrical cichlid fish Perissodus microlepis

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RAFFINI, Francesca, 2018. Exploring the origin and maintenance of biodiversity : insights from the bilaterally asymmetrical cichlid fish Perissodus microlepis [Dissertation]. Konstanz: University of Konstanz

@phdthesis{Raffini2018Explo-41634, title={Exploring the origin and maintenance of biodiversity : insights from the bilaterally asymmetrical cichlid fish Perissodus microlepis}, year={2018}, author={Raffini, Francesca}, address={Konstanz}, school={Universität Konstanz} }

2018-02-28T10:04:57Z Raffini, Francesca 2018 terms-of-use Exploring the origin and maintenance of biodiversity : insights from the bilaterally asymmetrical cichlid fish Perissodus microlepis 2018-02-28T10:04:57Z Raffini, Francesca eng How the striking diversity of life forms and their adaptations to the environment they inhabit emerge and are maintained in natural populations are largely unaddressed questions. An outstanding natural system to uncover the processes underlying biodiversity and adaptation are cichlid fishes, famously known for their spectacular rapid adaptive radiation. In a relatively short timeframe, they have evolved an extraordinary phenotypic diversity reflecting adaptations to often very narrow niches. Cichlids also comprise notable cases of stable polymorphisms, such as mouth asymmetry in the scale-eating cichlid fish Perissodus microlepis from Lake Tanganyika (Chapter I). Here, individuals with left- and right-bending mouth are found in sympatry in approximately equal frequencies. This morphological asymmetry is accompanied by lateralized foraging behavior: left individuals preferentially feed on the scales of the right side of its prey fish, and the opposite is true for the right morph. P. microlepis became a textbook model of extreme adaptation by ecological specialization and negative frequency-dependent selection via prey-predator interactions, that is thought to maintain this polymorphism over time. However, several contradicting findings and unaddressed questions emerged in the last years, challenging our understanding of this model. Knowledge on the morphological and developmental basis of this stable polymorphism, as well as the mechanisms that determine and drive intra-specific variation in this fish remain largely incomplete.<br />In Chapter II, I present an overview of the current knowledge on P. microlepis’ polymorphism, which has repeatedly attracted and puzzled biologists. I introduce the most recent findings towards understanding the basis of such a remarkable adaptation. This review shows existing evidence and gaps in uncovering the genetic and non-genetic factors influencing mouth asymmetry, and the association between morphological, behavioral and cerebral asymmetry. I highlight the most important unanswered questions, which represent the core of this Ph.D. research.<br />The first unsolved issue that is addressed in this thesis is the genetic basis underlying laterality in P. microlepis. A previously suggested simple genetic model of maintenance of a stable polymorphism has been criticized on multiple grounds recently. Chapter III elucidates whether mouth asymmetry has a significant genetic basis, and if its genomic architecture consists of a single/few or multiple loci. Using wild-caught fish and high-throughput DNA sequencing data, a novel array of single nucleotide polymorphism (SNP) markers is developed by ddRAD sequencing (ddRADseq) and the use of pooled DNA samples (PoolSeq), obtaining more than 155,000 (ddRADseq) and 3,900,000 (PoolSeq) SNPs. Among these, one (ddRAD) SNP, and 38 or 378 (PoolSeq) windows show differentiated allele frequencies between the left and right mouth morph, after accounting for spurious associations due to geographic structuring. These SNPs identify candidate genomic regions that potentially contain genes affecting or regulating this trait. Interestingly, these loci include genes related to immunity, ion transporters and cell adhesion proteins. Immunity genes are renowned to be potent drivers of divergence in fish even in sympatry. The other genes are known to be part of the mechanism regulating the early establishment of the left-right pattern during embryogenesis. Particularly, protocadherins are involved in neuronal network formation; they may play a central role in P. microlepis’ asymmetry, especially in behavioral lateralization. These findings clarify that this interesting trait has a genetic basis that is likely to be influenced by multiple loci, contributing to a greater understanding of the genetic determinants of left-right asymmetries.<br />Mouth asymmetry in P. microlepis has been recently observed to have a unimodal rather than a bimodal distribution, potentially indicating an effect of non-genetic factors on this trait, in line with previous evidence of phenotypic plasticity. Chapter IV explores the influence of environmental cues on asymmetry, another unclear issue. Particularly, it proposes that this unimodal distribution could result from the concerted effects of a sgenetic basis and a phenotypically plastic response due to feeding experience. This hypothesis is approached by validating the candidate SNP associated to mouth asymmetry identified by ddRADseq (Chapter III), analyzing inter-individual variation in feeding behavior using stable isotope analyses, and testing their association with mouth asymmetry. These results suggest that this polymorphism is shaped by both genes, including the candidate ddRAD locus, and non-genetic triggers, possibly due to inter-individual random and non-random variation in feeding behavior. This chapter introduces a first hypothesis linking genetic and environmental determination, and potentially explaining the simultaneous maintenance of left, right, asymmetric and symmetric mouth phenotypes in this outstanding cichlid fish.<br />Chapter V provides a more comprehensive analysis of aspects of the biology of this fish, focusing on cues that can be critical to understand its polymorphism but have been largely overlooked. Here, patterns of body shape and neutral genome-wide genetic diversity across geographic space, and the presence of asymmetry in eye size in relation to mouth are investigated using advanced genomic and geometric morphometrics approaches. This part of my thesis shows the presence of restrictions to gene flow across the distribution range of this species, which might have important implications on the determination and maintenance of asymmetry, such as the possibility that its genetic basis could vary among locations. Additionally, asymmetry in mouth and eye are significantly associated, potentially suggesting a mechanism linking morphological, behavioral and cerebral laterality. Results from this chapter highlight the importance of interactions among traits - including at the genetic level - and variation in geographic space to understand the evolution and maintenance of this and other stable polymorphisms.<br />An overview of tools that can be beneficial for studies that aim to bridge the gap between genotype or environmental cues and phenotype of potentially adaptive traits, such as mouth asymmetry, is presented in Chapter VI. A special focus is placed on the identification of signatures of balancing selection, a mode of selection that has been scarcely studied but can play a central role in evolutionary processes, particularly adaptation. I outline some pitfalls that limit their application to the study of P. microlepis and other non-model systems. I emphasize the importance of using integrative approaches that analyze polygenic, environmental and epigenetic variation in real populations to aid a comprehensive understanding of evolutionarily important phenotypes.<br />In conclusion, my Ph.D. research combines genetic, genomic, morphological and ecological analyses to enlighten how stable polymorphisms are produced and maintained in natural populations, i.e., what are the processes underlying biological diversity and adaptation. It clarifies the relative importance of genetic and environmental factors affecting mouth asymmetry in P. microlepis, and identifies structures and interactions possibly contributing to this polymorphism. These findings add to the growing support for a quantitative nature of this trait, propose candidate genes responsible for laterality, and emphasize the importance of jointly considering genetic, internal and external non-genetic triggers and interactions. This study contributes towards illuminating long-standing questions on asymmetry determination, and ultimately to our understanding of the processes leading to the incomparable biological diversity.

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