Genes Integral to the Reproductive Function of Male Reproductive Tissues Drive Heterogeneity in Evolutionary Rates in Japanese Quail

Early comparative genomics studies originally uncovered a nonintuitive pattern; genes involved in reproduction appeared to evolve more rapidly than other classes of genes. Currently, the emerging consensus is that genes encoding reproductive proteins evolve under variable selective pressures, produc...

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Main Authors: Findley R. Finseth, Richard G. Harrison
Format: Article
Language:English
Published: Oxford University Press 2018-01-01
Series:G3: Genes, Genomes, Genetics
Subjects:
Online Access:http://g3journal.org/lookup/doi/10.1534/g3.117.300095
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spelling doaj-f41ad9dadd3c4a71963cc07b74cb37c02021-07-02T07:19:43ZengOxford University PressG3: Genes, Genomes, Genetics2160-18362018-01-0181395110.1534/g3.117.3000955Genes Integral to the Reproductive Function of Male Reproductive Tissues Drive Heterogeneity in Evolutionary Rates in Japanese QuailFindley R. FinsethRichard G. HarrisonEarly comparative genomics studies originally uncovered a nonintuitive pattern; genes involved in reproduction appeared to evolve more rapidly than other classes of genes. Currently, the emerging consensus is that genes encoding reproductive proteins evolve under variable selective pressures, producing more heterogeneous divergence patterns than previously appreciated. Here, we investigate a facet of that heterogeneity and explore the factors that drive male reproductive tissue-based heterogeneity in evolutionary rates. In Japanese quail (Coturnix japonica), genes with enriched expression in the testes evolve much more rapidly than those enriched in the foam gland (FG), a novel gland that secretes an airy foam that males transfer to females during mating. We compared molecular evolutionary patterns among (1) genes with induced expression in breeding vs. wintering conditions for both tissues and (2) genes that encode foam proteins (FPs) vs. those with varying degrees of expression specificity in the FG. We report two major findings. First, genes upregulated in breeding condition testes evolve exceptionally rapidly, while those induced in breeding condition FGs evolve slowly. These differences hold even after correcting for hormonally-dependent gene expression and chromosomal location. Second, genes encoding FPs are extremely conserved in terms of gene identity and sequence. Together, these finding suggest that genes involved in the reproductive function of each tissue drive the marked rate of heterogeneity.http://g3journal.org/lookup/doi/10.1534/g3.117.300095reproductive proteinRNA-Seqproteomicscomparative genomicsJapanese quail
collection DOAJ
language English
format Article
sources DOAJ
author Findley R. Finseth
Richard G. Harrison
spellingShingle Findley R. Finseth
Richard G. Harrison
Genes Integral to the Reproductive Function of Male Reproductive Tissues Drive Heterogeneity in Evolutionary Rates in Japanese Quail
G3: Genes, Genomes, Genetics
reproductive protein
RNA-Seq
proteomics
comparative genomics
Japanese quail
author_facet Findley R. Finseth
Richard G. Harrison
author_sort Findley R. Finseth
title Genes Integral to the Reproductive Function of Male Reproductive Tissues Drive Heterogeneity in Evolutionary Rates in Japanese Quail
title_short Genes Integral to the Reproductive Function of Male Reproductive Tissues Drive Heterogeneity in Evolutionary Rates in Japanese Quail
title_full Genes Integral to the Reproductive Function of Male Reproductive Tissues Drive Heterogeneity in Evolutionary Rates in Japanese Quail
title_fullStr Genes Integral to the Reproductive Function of Male Reproductive Tissues Drive Heterogeneity in Evolutionary Rates in Japanese Quail
title_full_unstemmed Genes Integral to the Reproductive Function of Male Reproductive Tissues Drive Heterogeneity in Evolutionary Rates in Japanese Quail
title_sort genes integral to the reproductive function of male reproductive tissues drive heterogeneity in evolutionary rates in japanese quail
publisher Oxford University Press
series G3: Genes, Genomes, Genetics
issn 2160-1836
publishDate 2018-01-01
description Early comparative genomics studies originally uncovered a nonintuitive pattern; genes involved in reproduction appeared to evolve more rapidly than other classes of genes. Currently, the emerging consensus is that genes encoding reproductive proteins evolve under variable selective pressures, producing more heterogeneous divergence patterns than previously appreciated. Here, we investigate a facet of that heterogeneity and explore the factors that drive male reproductive tissue-based heterogeneity in evolutionary rates. In Japanese quail (Coturnix japonica), genes with enriched expression in the testes evolve much more rapidly than those enriched in the foam gland (FG), a novel gland that secretes an airy foam that males transfer to females during mating. We compared molecular evolutionary patterns among (1) genes with induced expression in breeding vs. wintering conditions for both tissues and (2) genes that encode foam proteins (FPs) vs. those with varying degrees of expression specificity in the FG. We report two major findings. First, genes upregulated in breeding condition testes evolve exceptionally rapidly, while those induced in breeding condition FGs evolve slowly. These differences hold even after correcting for hormonally-dependent gene expression and chromosomal location. Second, genes encoding FPs are extremely conserved in terms of gene identity and sequence. Together, these finding suggest that genes involved in the reproductive function of each tissue drive the marked rate of heterogeneity.
topic reproductive protein
RNA-Seq
proteomics
comparative genomics
Japanese quail
url http://g3journal.org/lookup/doi/10.1534/g3.117.300095
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