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Open AccessArticle

Patterns and Constraints in the Evolution of Sperm Individualization Genes in Insects, with an Emphasis on Beetles

1
Animal Biodiversity and Evolution, Institute of Evolutionary Biology (CSIC-Universitat Pompeu Fabra), 08003 Barcelona, Spain
2
Center for Molecular Biodiversity Research, Zoological Research Museum Alexander Koenig, 53113 Bonn, Germany
3
Center for Biodiversity Research, Department of Biological Sciences, University of Memphis, Memphis, TN 38152, USA
4
Department of Entomology, College of Plant Protection, China Agricultural University, Beijing 100193, China
*
Author to whom correspondence should be addressed.
Genes 2019, 10(10), 776; https://doi.org/10.3390/genes10100776
Received: 24 August 2019 / Revised: 20 September 2019 / Accepted: 1 October 2019 / Published: 4 October 2019
(This article belongs to the Section Population and Evolutionary Genetics and Genomics)
Gene expression profiles can change dramatically between sexes and sex bias may contribute specific macroevolutionary dynamics for sex-biased genes. However, these dynamics are poorly understood at large evolutionary scales due to the paucity of studies that have assessed orthology and functional homology for sex-biased genes and the pleiotropic effects possibly constraining their evolutionary potential. Here, we explore the correlation of sex-biased expression with macroevolutionary processes that are associated with sex-biased genes, including duplications and accelerated evolutionary rates. Specifically, we examined these traits in a group of 44 genes that orchestrate sperm individualization during spermatogenesis, with both unbiased and sex-biased expression. We studied these genes in the broad evolutionary framework of the Insecta, with a particular focus on beetles (order Coleoptera). We studied data mined from 119 insect genomes, including 6 beetle models, and from 19 additional beetle transcriptomes. For the subset of physically and/or genetically interacting proteins, we also analyzed how their network structure may condition the mode of gene evolution. The collection of genes was highly heterogeneous in duplication status, evolutionary rates, and rate stability, but there was statistical evidence for sex bias correlated with faster evolutionary rates, consistent with theoretical predictions. Faster rates were also correlated with clocklike (insect amino acids) and non-clocklike (beetle nucleotides) substitution patterns in these genes. Statistical associations (higher rates for central nodes) or lack thereof (centrality of duplicated genes) were in contrast to some current evolutionary hypotheses, highlighting the need for more research on these topics.
Keywords: Coleoptera; evolutionary rates; gene network; Insecta; phylogenetic inference; sex-biased genes Coleoptera; evolutionary rates; gene network; Insecta; phylogenetic inference; sex-biased genes
MDPI and ACS Style

Vizán-Rico, H.I.; Mayer, C.; Petersen, M.; McKenna, D.D.; Zhou, X.; Gómez-Zurita, J. Patterns and Constraints in the Evolution of Sperm Individualization Genes in Insects, with an Emphasis on Beetles. Genes 2019, 10, 776.

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