Patterns and Constraints in the Evolution of Sperm Individualization Genes in Insects, with an Emphasis on Beetles
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 ho...
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doaj-e5267b93aa5c4994ae3c8508e9cd93e62020-11-24T21:55:32ZengMDPI AGGenes2073-44252019-10-01101077610.3390/genes10100776genes10100776Patterns and Constraints in the Evolution of Sperm Individualization Genes in Insects, with an Emphasis on BeetlesHelena I. Vizán-Rico0Christoph Mayer1Malte Petersen2Duane D. McKenna3Xin Zhou4Jesús Gómez-Zurita5Animal Biodiversity and Evolution, Institute of Evolutionary Biology (CSIC-Universitat Pompeu Fabra), 08003 Barcelona, SpainCenter for Molecular Biodiversity Research, Zoological Research Museum Alexander Koenig, 53113 Bonn, GermanyCenter for Molecular Biodiversity Research, Zoological Research Museum Alexander Koenig, 53113 Bonn, GermanyCenter for Biodiversity Research, Department of Biological Sciences, University of Memphis, Memphis, TN 38152, USADepartment of Entomology, College of Plant Protection, China Agricultural University, Beijing 100193, ChinaAnimal Biodiversity and Evolution, Institute of Evolutionary Biology (CSIC-Universitat Pompeu Fabra), 08003 Barcelona, SpainGene 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.https://www.mdpi.com/2073-4425/10/10/776coleopteraevolutionary ratesgene networkinsectaphylogenetic inferencesex-biased genes |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Helena I. Vizán-Rico Christoph Mayer Malte Petersen Duane D. McKenna Xin Zhou Jesús Gómez-Zurita |
spellingShingle |
Helena I. Vizán-Rico Christoph Mayer Malte Petersen Duane D. McKenna Xin Zhou Jesús Gómez-Zurita Patterns and Constraints in the Evolution of Sperm Individualization Genes in Insects, with an Emphasis on Beetles Genes coleoptera evolutionary rates gene network insecta phylogenetic inference sex-biased genes |
author_facet |
Helena I. Vizán-Rico Christoph Mayer Malte Petersen Duane D. McKenna Xin Zhou Jesús Gómez-Zurita |
author_sort |
Helena I. Vizán-Rico |
title |
Patterns and Constraints in the Evolution of Sperm Individualization Genes in Insects, with an Emphasis on Beetles |
title_short |
Patterns and Constraints in the Evolution of Sperm Individualization Genes in Insects, with an Emphasis on Beetles |
title_full |
Patterns and Constraints in the Evolution of Sperm Individualization Genes in Insects, with an Emphasis on Beetles |
title_fullStr |
Patterns and Constraints in the Evolution of Sperm Individualization Genes in Insects, with an Emphasis on Beetles |
title_full_unstemmed |
Patterns and Constraints in the Evolution of Sperm Individualization Genes in Insects, with an Emphasis on Beetles |
title_sort |
patterns and constraints in the evolution of sperm individualization genes in insects, with an emphasis on beetles |
publisher |
MDPI AG |
series |
Genes |
issn |
2073-4425 |
publishDate |
2019-10-01 |
description |
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. |
topic |
coleoptera evolutionary rates gene network insecta phylogenetic inference sex-biased genes |
url |
https://www.mdpi.com/2073-4425/10/10/776 |
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