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      Duplications in Corneous Beta Protein Genes and the Evolution of Gecko Adhesion

      1 , 2 , 3
      Integrative and Comparative Biology
      Oxford University Press (OUP)

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          Abstract

          Corneous proteins are an important component of the tetrapod integument. Duplication and diversification of keratins and associated proteins are linked with the origin of most novel integumentary structures like mammalian hair, avian feathers, and scutes covering turtle shells. Accordingly, the loss of integumentary structures often coincides with the loss of genes encoding keratin and associated proteins. For example, many hair keratins in dolphins and whales have become pseudogenes. The adhesive setae of geckos and anoles are composed of both intermediate filament keratins (IF-keratins, formerly known as alpha-keratins) and corneous beta‐proteins (CBPs, formerly known as beta-keratins) and recent whole genome assemblies of two gecko species and an anole uncovered duplications in seta-specific CBPs in each of these lineages. While anoles evolved adhesive toepads just once, there are two competing hypotheses about the origin(s) of digital adhesion in geckos involving either a single origin or multiple origins. Using data from three published gecko genomes, I examine CBP gene evolution in geckos and find support for a hypothesis where CBP gene duplications are associated with the repeated evolution of digital adhesion. Although these results are preliminary, I discuss how additional gecko genome assemblies, combined with phylogenies of keratin and associated protein genes and gene duplication models, can provide rigorous tests of several hypotheses related to gecko CBP evolution. This includes a taxon sampling strategy for sequencing and assembly of gecko genomes that could help resolve competing hypotheses surrounding the origin(s) of digital adhesion.

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          Most cited references62

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          Estimating gene gain and loss rates in the presence of error in genome assembly and annotation using CAFE 3.

          Current sequencing methods produce large amounts of data, but genome assemblies constructed from these data are often fragmented and incomplete. Incomplete and error-filled assemblies result in many annotation errors, especially in the number of genes present in a genome. This means that methods attempting to estimate rates of gene duplication and loss often will be misled by such errors and that rates of gene family evolution will be consistently overestimated. Here, we present a method that takes these errors into account, allowing one to accurately infer rates of gene gain and loss among genomes even with low assembly and annotation quality. The method is implemented in the newest version of the software package CAFE, along with several other novel features. We demonstrate the accuracy of the method with extensive simulations and reanalyze several previously published data sets. Our results show that errors in genome annotation do lead to higher inferred rates of gene gain and loss but that CAFE 3 sufficiently accounts for these errors to provide accurate estimates of important evolutionary parameters.
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            Model inadequacy and mistaken inferences of trait-dependent speciation.

            Species richness varies widely across the tree of life, and there is great interest in identifying ecological, geographic, and other factors that affect rates of species proliferation. Recent methods for explicitly modeling the relationships among character states, speciation rates, and extinction rates on phylogenetic trees- BiSSE, QuaSSE, GeoSSE, and related models-have been widely used to test hypotheses about character state-dependent diversification rates. Here, we document the disconcerting ease with which neutral traits are inferred to have statistically significant associations with speciation rate. We first demonstrate this unfortunate effect for a known model assumption violation: shifts in speciation rate associated with a character not included in the model. We further show that for many empirical phylogenies, characters simulated in the absence of state-dependent diversification exhibit an even higher Type I error rate, indicating that the method is susceptible to additional, unknown model inadequacies. For traits that evolve slowly, the root cause appears to be a statistical framework that does not require replicated shifts in character state and diversification. However, spurious associations between character state and speciation rate arise even for traits that lack phylogenetic signal, suggesting that phylogenetic pseudoreplication alone cannot fully explain the problem. The surprising severity of this phenomenon suggests that many trait-diversification relationships reported in the literature may not be real. More generally, we highlight the need for diagnosing and understanding the consequences of model inadequacy in phylogenetic comparative methods.
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              The role of lineage-specific gene family expansion in the evolution of eukaryotes.

              A computational procedure was developed for systematic detection of lineage-specific expansions (LSEs) of protein families in sequenced genomes and applied to obtain a census of LSEs in five eukaryotic species, the yeasts Saccharomyces cerevisiae and Schizosaccharomyces pombe, the nematode Caenorhabditis elegans, the fruit fly Drosophila melanogaster, and the green plant Arabidopsis thaliana. A significant fraction of the proteins encoded in each of these genomes, up to 80% in A. thaliana, belong to LSEs. Many paralogous gene families in each of the analyzed species are almost entirely comprised of LSEs, indicating that their diversification occurred after the divergence of the major lineages of the eukaryotic crown group. The LSEs show readily discernible patterns of protein functions. The functional categories most prone to LSE are structural proteins, enzymes involved in an organism's response to pathogens and environmental stress, and various components of signaling pathways responsible for specificity, including ubiquitin ligase E3 subunits and transcription factors. The functions of several previously uncharacterized, vastly expanded protein families were predicted through in-depth protein sequence analysis, for example, small-molecule kinases and methylases that are expanded independently in the fly and in the nematode. The functions of several other major LSEs remain mysterious; these protein families are attractive targets for experimental discovery of novel, lineage-specific functions in eukaryotes. LSEs seem to be one of the principal means of adaptation and one of the most important sources of organizational and regulatory diversity in crown-group eukaryotes.
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                Author and article information

                Journal
                Integrative and Comparative Biology
                Oxford University Press (OUP)
                1540-7063
                1557-7023
                July 2019
                July 01 2019
                April 27 2019
                July 2019
                July 01 2019
                April 27 2019
                : 59
                : 1
                : 193-202
                Affiliations
                [1 ]Department of Biological Sciences, Marquette University, Milwaukee, WI 53201, USA
                [2 ]Bell Museum of Natural History, University of Minnesota, Saint Paul, MN 55113, USA
                [3 ]Milwaukee Public Museum, Milwaukee, WI 53233, USA
                Article
                10.1093/icb/icz010
                30895301
                968c6a1b-c534-4b74-a79d-25a7568a817c
                © 2019

                https://academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model

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