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      Divergent Allometric Trajectories in Gene Expression and Coexpression Produce Species Differences in Sympatrically Speciating Midas Cichlid Fish

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          Abstract

          The mechanisms of speciation without geographic isolation (i.e., sympatric speciation) remain debated. This is due in part to the fact that the genomic landscape that could promote or hinder species divergence in the presence of gene flow is still largely unknown. However, intensive research is now centered on understanding the genetic architecture of adaptive traits associated with this process as well as how gene expression might affect these traits. Here, using RNA-Seq data, we investigated gene expression of sympatrically speciating benthic and limnetic Neotropical cichlid fishes at two developmental stages. First, we identified groups of coexpressed genes (modules) at each stage. Although there are a few large and well-preserved modules, most of the other modules are not preserved across life stages. Second, we show that later in development more and larger coexpression modules are associated with divergence between benthic and limnetic fish compared with the earlier life stage. This divergence between benthic and limnetic fish in coexpression mirrors divergence in overall expression between benthic and limnetic fish, which is more pronounced later in life. Our results reveal that already at 1-day posthatch benthic and limnetic fish diverge in (co)expression, and that this divergence becomes more substantial when fish are free-swimming but still unlikely to have divergent swimming and feeding habits. More importantly, our study describes how the coexpression of several genes through development, as opposed to individual genes, is associated with benthic–limnetic species differences, and how two morphogenetic trajectories diverge as fish grow older.

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          Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing

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            Sympatric speciation in Nicaraguan crater lake cichlid fish.

            Sympatric speciation, the formation of species in the absence of geographical barriers, remains one of the most contentious concepts in evolutionary biology. Although speciation under sympatric conditions seems theoretically possible, empirical studies are scarce and only a few credible examples of sympatric speciation exist. Here we present a convincing case of sympatric speciation in the Midas cichlid species complex (Amphilophus sp.) in a young and small volcanic crater lake in Nicaragua. Our study includes phylogeographic, population-genetic (based on mitochondrial DNA, microsatellites and amplified fragment length polymorphisms), morphometric and ecological analyses. We find, first, that crater Lake Apoyo was seeded only once by the ancestral high-bodied benthic species Amphilophus citrinellus, the most common cichlid species in the area; second, that a new elongated limnetic species (Amphilophus zaliosus) evolved in Lake Apoyo from the ancestral species (A. citrinellus) within less than approximately 10,000 yr; third, that the two species in Lake Apoyo are reproductively isolated; and fourth, that the two species are eco-morphologically distinct.
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              Comparative studies of gene expression and the evolution of gene regulation.

              The hypothesis that differences in gene regulation have an important role in speciation and adaptation is more than 40 years old. With the advent of new sequencing technologies, we are able to characterize and study gene expression levels and associated regulatory mechanisms in a large number of individuals and species at an unprecedented resolution and scale. We have thus gained new insights into the evolutionary pressures that shape gene expression levels and have developed an appreciation for the relative importance of evolutionary changes in different regulatory genetic and epigenetic mechanisms. The current challenge is to link gene regulatory changes to adaptive evolution of complex phenotypes. Here we mainly focus on comparative studies in primates and how they are complemented by studies in model organisms.
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                Author and article information

                Contributors
                Role: Associate Editor
                Journal
                Genome Biol Evol
                Genome Biol Evol
                gbe
                Genome Biology and Evolution
                Oxford University Press
                1759-6653
                June 2019
                24 May 2019
                24 May 2019
                : 11
                : 6
                : 1644-1657
                Affiliations
                [1 ]Department of Biology, University of Konstanz, Germany
                [2 ]Institut de Biologie de l'École Normale Supérieure (IBENS), École Normale Supérieure, CNRS UMR 8197, Paris, France
                Author notes
                Corresponding author: E-mail: paolo.franchini@ 123456uni-konstanz.de .
                Author information
                http://orcid.org/0000-0002-8184-1463
                Article
                evz108
                10.1093/gbe/evz108
                6563553
                31124568
                de81217f-9e55-4486-9359-229aad36c3ae
                © The Author(s) 2019. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 17 May 2019
                Page count
                Pages: 14
                Funding
                Funded by: Deutsche Forschungsgemeinschaft Research
                Award ID: FR 3399/1–1
                Funded by: European Research Council 10.13039/100010663
                Award ID: 293700
                Categories
                Research Article

                Genetics
                rna-seq,coexpression,wgcna,benthic–limnetic divergence,evolvability,modules
                Genetics
                rna-seq, coexpression, wgcna, benthic–limnetic divergence, evolvability, modules

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