Rapid Gene Family Evolution of a Nematode Sperm Protein Despite Sequence Hyper-conservation

Reproductive proteins are often observed to be the most rapidly evolving elements within eukaryotic genomes. The major sperm protein (MSP) is unique to the phylum Nematoda and is required for proper sperm locomotion and fertilization. Here, we annotate the MSP gene family and analyze their molecular...

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Main Authors: Katja R. Kasimatis, Patrick C. Phillips
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/g3.117.300281
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author Katja R. Kasimatis
Patrick C. Phillips
author_facet Katja R. Kasimatis
Patrick C. Phillips
author_sort Katja R. Kasimatis
collection DOAJ
description Reproductive proteins are often observed to be the most rapidly evolving elements within eukaryotic genomes. The major sperm protein (MSP) is unique to the phylum Nematoda and is required for proper sperm locomotion and fertilization. Here, we annotate the MSP gene family and analyze their molecular evolution in 10 representative species across Nematoda. We show that MSPs are hyper-conserved across the phylum, having maintained an amino acid sequence identity of 83.5–97.7% for over 500 million years. This extremely slow rate of evolution makes MSPs some of the most highly conserved genes yet identified. However, at the gene family level, we show hyper-variability in both gene copy number and genomic position within species, suggesting rapid, lineage-specific gene family evolution. Additionally, we find evidence that extensive gene conversion contributes to the maintenance of sequence identity within chromosome-level clusters of MSP genes. Thus, while not conforming to the standard expectation for the evolution of reproductive proteins, our analysis of the molecular evolution of the MSP gene family is nonetheless consistent with the widely repeatable observation that reproductive proteins evolve rapidly, in this case in terms of the genomic properties of gene structure, copy number, and genomic organization. This unusual evolutionary pattern is likely generated by strong pleiotropic constraints acting on these genes at the sequence level, balanced against expansion at the level of the whole gene family.
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spelling doaj.art-e35f326605644df597cb25fdfcd3ba972022-12-21T22:39:25ZengOxford University PressG3: Genes, Genomes, Genetics2160-18362018-01-018135336210.1534/g3.117.30028131Rapid Gene Family Evolution of a Nematode Sperm Protein Despite Sequence Hyper-conservationKatja R. KasimatisPatrick C. PhillipsReproductive proteins are often observed to be the most rapidly evolving elements within eukaryotic genomes. The major sperm protein (MSP) is unique to the phylum Nematoda and is required for proper sperm locomotion and fertilization. Here, we annotate the MSP gene family and analyze their molecular evolution in 10 representative species across Nematoda. We show that MSPs are hyper-conserved across the phylum, having maintained an amino acid sequence identity of 83.5–97.7% for over 500 million years. This extremely slow rate of evolution makes MSPs some of the most highly conserved genes yet identified. However, at the gene family level, we show hyper-variability in both gene copy number and genomic position within species, suggesting rapid, lineage-specific gene family evolution. Additionally, we find evidence that extensive gene conversion contributes to the maintenance of sequence identity within chromosome-level clusters of MSP genes. Thus, while not conforming to the standard expectation for the evolution of reproductive proteins, our analysis of the molecular evolution of the MSP gene family is nonetheless consistent with the widely repeatable observation that reproductive proteins evolve rapidly, in this case in terms of the genomic properties of gene structure, copy number, and genomic organization. This unusual evolutionary pattern is likely generated by strong pleiotropic constraints acting on these genes at the sequence level, balanced against expansion at the level of the whole gene family.http://g3journal.org/lookup/doi/10.1534/g3.117.300281molecular evolutiongene family evolutionreproductive proteinsnematodes
spellingShingle Katja R. Kasimatis
Patrick C. Phillips
Rapid Gene Family Evolution of a Nematode Sperm Protein Despite Sequence Hyper-conservation
G3: Genes, Genomes, Genetics
molecular evolution
gene family evolution
reproductive proteins
nematodes
title Rapid Gene Family Evolution of a Nematode Sperm Protein Despite Sequence Hyper-conservation
title_full Rapid Gene Family Evolution of a Nematode Sperm Protein Despite Sequence Hyper-conservation
title_fullStr Rapid Gene Family Evolution of a Nematode Sperm Protein Despite Sequence Hyper-conservation
title_full_unstemmed Rapid Gene Family Evolution of a Nematode Sperm Protein Despite Sequence Hyper-conservation
title_short Rapid Gene Family Evolution of a Nematode Sperm Protein Despite Sequence Hyper-conservation
title_sort rapid gene family evolution of a nematode sperm protein despite sequence hyper conservation
topic molecular evolution
gene family evolution
reproductive proteins
nematodes
url http://g3journal.org/lookup/doi/10.1534/g3.117.300281
work_keys_str_mv AT katjarkasimatis rapidgenefamilyevolutionofanematodespermproteindespitesequencehyperconservation
AT patrickcphillips rapidgenefamilyevolutionofanematodespermproteindespitesequencehyperconservation