Genetic support for random mating between left and right‐mouth morphs in the dimorphic scale‐eating cichlid fish <i>Perissodus microlepis</i> from Lake Tanganyika

Lee, Hyuk Je; Pittlik, Silke; Jones, Julia C.; Salzburger, Walter; Barluenga, Marta; Meyer, Axel

doi:10.1111/j.1095-8649.2010.02620.x

Cited by 19 publications

(65 citation statements)

References 45 publications

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“…¼ 1.21 cm). None of the five sampling locations showed deviations from an equal ratio of R-to L-morphs (table 1), corroborating the earlier hypothesis of equal abundance [5,11].…”

Section: Results (A) Equal Abundance Of Mouth Morphs and Random Matinsupporting

confidence: 86%

“…[19]. These new field data are consistent with our previous work that revealed no genetic differentiation between morphs based on both, mitochondrial and nuclear DNA markers, but that provided genetic support for the random mating hypothesis [11]. Hypothetical selective advantages for breeding assortatively or disassortatively were thus not reflected or detected by genetic analyses.…”

Section: Discussionsupporting

confidence: 89%

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Mouth asymmetry in the textbook example of scale-eating cichlid fish is not a discrete dimorphism after all

2012

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Individuals of the scale-eating cichlid fish, Perissodus microlepis, from Lake Tanganyika tend to have remarkably asymmetric heads that are either left-bending or right-bending. The 'left' morph opens its mouth markedly towards the left and preferentially feeds on the scales from the right-hand side of its victim fish, and the 'right' morph bites scales from the victims' left-hand side. This striking dimorphism made these fish a textbook example of their astonishing degree of ecological specialization and as one of the few known incidences of negative frequency-dependent selection acting on an asymmetric morphological trait, where left and right forms are equally frequent within a species. We investigated the degree and the shape of the frequency distribution of head asymmetry in P. microlepis to test whether the variation conforms to a discrete dimorphism, as generally assumed. In both adult and juvenile fish, mouth asymmetry appeared to be continuously and unimodally distributed with no clear evidence for a discrete dimorphism. Mixture analyses did not reveal evidence of a discrete or even strong dimorphism. These results raise doubts about previous claims, as reported in textbooks, that head variation in P. microlepis represents a discrete dimorphism of left-and right-bending forms. Based on extensive field sampling that excluded ambiguous (i.e. symmetric or weakly asymmetric) individual adults, we found that left and right morphs occur in equal abundance in five populations. Moreover, mate pairing for 51 wild-caught pairs was random with regard to head laterality, calling into question reports that this laterality is maintained through disassortative mating.

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“…¼ 1.21 cm). None of the five sampling locations showed deviations from an equal ratio of R-to L-morphs (table 1), corroborating the earlier hypothesis of equal abundance [5,11].…”

Section: Results (A) Equal Abundance Of Mouth Morphs and Random Matinsupporting

confidence: 86%

Section: Discussionsupporting

confidence: 89%

Mouth asymmetry in the textbook example of scale-eating cichlid fish is not a discrete dimorphism after all

2012

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“…While previous studies failed to validate a former candidate locus (UNH2101; Lee et al., 2015, 2010; Stewart & Albertson, 2010 but note the use of different methods to estimate asymmetry), here, we confirmed the association between the locus located in a genomic region containing immunoglobulin genes and mouth polymorphism. Specifically, the SNP 56537‐113 is related to mouth asymmetry whether this is expressed as a continuous trait (mouth bending angle, this study) or as a categorical variable (L and R morphs, Raffini et al., 2017).…”

Section: Discussionsupporting

confidence: 84%

“…Previous studies suggested random or disassortative mating as well as negative frequency‐dependent selection in P. microlepis (Hori, 1993; Kusche et al., 2012; Lee et al., 2010; Takahashi & Hori, 2008 but see Raffini et al., 2017). Restrictions to gene flow linked to geography have been identified in the distribution range of this species (Koblmüller et al., 2009; Raffini et al., 2017, in press); however, we observed a significant genotype‐phenotype relationship also when controlling for geography (Raffini et al., 2017, this study).…”

Section: Discussionmentioning

confidence: 99%

“…This leads to the question: which regions of the genome contain the gene(s) responsible for asymmetry? A microsatellite locus was suggested to be linked to a putative laterality gene (Stewart & Albertson, 2010), but subsequent studies failed to confirm this association (Lee et al., 2010, 2015). More recently, we conducted a genome‐wide study that identified several SNPs potentially related to mouth asymmetry (Raffini et al., 2017).…”

Section: Introductionmentioning

confidence: 99%

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Gene(s) and individual feeding behavior: Exploring eco‐evolutionary dynamics underlying left‐right asymmetry in the scale‐eating cichlid fishPerissodus microlepis

Raffini

Fruciano

Meyer

2018

Ecology and Evolution

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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.

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Genetic and environmental effects on the morphological asymmetry in the scale‐eating cichlid fish, Perissodus microlepis

Lee

Heim

Meyer

2015

Ecology and Evolution

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The scale‐eating cichlid fish, Perissodus microlepis, from Lake Tanganyika are a well‐known example of an asymmetry dimorphism because the mouth/head is either left‐bending or right‐bending. However, how strongly its pronounced morphological laterality is affected by genetic and environmental factors remains unclear. Using quantitative assessments of mouth asymmetry, we investigated its origin by estimating narrow‐sense heritability (h 2) using midparent–offspring regression. The heritability estimates [field estimate: h 2 = 0.22 ± 0.06, P = 0.013; laboratory estimate: h 2 = 0.18 ± 0.05, P = 0.004] suggest that although variation in laterality has some additive genetic component, it is strongly environmentally influenced. Family‐level association analyses of a putative microsatellite marker that was claimed to be linked to gene(s) for laterality revealed no association of this locus with laterality. Moreover, the observed phenotype frequencies in offspring from parents of different phenotype combinations were not consistent with a previously suggested single‐locus two‐allele model, but they neither were able to reject with confidence a random asymmetry model. These results reconcile the disputed mechanisms for this textbook case of mouth asymmetry where both genetic and environmental factors contribute to this remarkable case of morphological asymmetry.

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Genetic support for random mating between left and right‐mouth morphs in the dimorphic scale‐eating cichlid fish Perissodus microlepis from Lake Tanganyika

Cited by 19 publications

References 45 publications

Mouth asymmetry in the textbook example of scale-eating cichlid fish is not a discrete dimorphism after all

Mouth asymmetry in the textbook example of scale-eating cichlid fish is not a discrete dimorphism after all

Gene(s) and individual feeding behavior: Exploring eco‐evolutionary dynamics underlying left‐right asymmetry in the scale‐eating cichlid fishPerissodus microlepis

Genetic and environmental effects on the morphological asymmetry in the scale‐eating cichlid fish, Perissodus microlepis

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