Gamete Recognition Gene Divergence Yields a Robust Eutherian Phylogeny across Taxonomic Levels

The extraordinary morphological diversity among extant mammals poses a challenge for studies of speciation, adaptation, molecular evolution, and reproductive isolation. Despite the recent wealth of molecular studies on mammalian phylogenetics, uncertainties remain surrounding both ancestral and more...

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Main Authors: Emma K. Roberts, Emily A. Wright, Asha E. Worsham, Daniel M. Hardy, Robert D. Bradley
Format: Article
Language:English
Published: MDPI AG 2023-11-01
Series:Diversity
Subjects:
Online Access:https://www.mdpi.com/1424-2818/15/11/1145
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author Emma K. Roberts
Emily A. Wright
Asha E. Worsham
Daniel M. Hardy
Robert D. Bradley
author_facet Emma K. Roberts
Emily A. Wright
Asha E. Worsham
Daniel M. Hardy
Robert D. Bradley
author_sort Emma K. Roberts
collection DOAJ
description The extraordinary morphological diversity among extant mammals poses a challenge for studies of speciation, adaptation, molecular evolution, and reproductive isolation. Despite the recent wealth of molecular studies on mammalian phylogenetics, uncertainties remain surrounding both ancestral and more recent divergence events that have proven difficult to resolve. Multi-gene datasets, especially including genes that are highly divergent, often provide increased support for higher-level affinities within Mammalia; however, such analyses require vast amounts of genomic sequence data and at times, intensive, high-performance computational effort. Furthermore, despite the large-scale efforts dedicated to comprehensive, multi-gene phylogenetic analyses using a combination of mitochondrial, nuclear, and other sequences (e.g., tRNA, ultra-conserved elements, and transposable elements), many relationships across Mammalia remain highly controversial. To offer another approach and provide a phylogenetic solution to this longstanding issue, here we present a phylogenetic tool based on a single reproductive molecular marker, zonadhesin (gene: <i>Zan</i>), one of two known mammalian speciation genes, which encodes the rapidly evolving sperm protein zonadhesin that mediates species-specific adhesion to the egg and thereby promotes reproductive isolation among placental mammals (Eutheria). Topological comparison of <i>Zan</i> Maximum Likelihood phylogenies to a nearly complete mammalian supertree confirmed <i>Zan</i>’s striking phylogenetic utility and resolution at both deeper and more terminal nodes in the placental mammalian phylogeny. This single gene marker yielded an equivalent and/or superiorly supported topology in comparison to a supertree generated using DNA sequences from a supermatrix of 31 genes from 5911 species (extinct and extant). Resolution achieved with this new phylogenetic approach provides unique insights into the divergence of both early and recent mammalian radiations. Finally, and perhaps most importantly, the utility of zonadhesin as a singular molecular marker was especially useful in clades where sufficient taxon sampling is impossible to achieve, and where only a subset of members of the mammalian species tree is available. The eutherian relationships presented here provide a foundation for future studies in the reconstruction of mammalian classifications, including reproductive isolation, hybridization, and biodiversification of species.
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spelling doaj.art-baea1ed2b7924d9292fee33ed89590fe2023-11-24T14:38:00ZengMDPI AGDiversity1424-28182023-11-011511114510.3390/d15111145Gamete Recognition Gene Divergence Yields a Robust Eutherian Phylogeny across Taxonomic LevelsEmma K. Roberts0Emily A. Wright1Asha E. Worsham2Daniel M. Hardy3Robert D. Bradley4Climate Center, and Department of Biological Sciences, Texas Tech University, Lubbock, TX 79409, USADepartment of Biological Sciences, Texas Tech University, Lubbock, TX 79409, USADepartment of Cell Biology & Biochemistry, Texas Tech University Health Sciences Center, Lubbock, TX 79430, USADepartment of Cell Biology & Biochemistry, Texas Tech University Health Sciences Center, Lubbock, TX 79430, USADepartment of Biological Sciences, and Natural Science Research Laboratory, Museum at Texas Tech University, Texas Tech University, Lubbock, TX 79409, USAThe extraordinary morphological diversity among extant mammals poses a challenge for studies of speciation, adaptation, molecular evolution, and reproductive isolation. Despite the recent wealth of molecular studies on mammalian phylogenetics, uncertainties remain surrounding both ancestral and more recent divergence events that have proven difficult to resolve. Multi-gene datasets, especially including genes that are highly divergent, often provide increased support for higher-level affinities within Mammalia; however, such analyses require vast amounts of genomic sequence data and at times, intensive, high-performance computational effort. Furthermore, despite the large-scale efforts dedicated to comprehensive, multi-gene phylogenetic analyses using a combination of mitochondrial, nuclear, and other sequences (e.g., tRNA, ultra-conserved elements, and transposable elements), many relationships across Mammalia remain highly controversial. To offer another approach and provide a phylogenetic solution to this longstanding issue, here we present a phylogenetic tool based on a single reproductive molecular marker, zonadhesin (gene: <i>Zan</i>), one of two known mammalian speciation genes, which encodes the rapidly evolving sperm protein zonadhesin that mediates species-specific adhesion to the egg and thereby promotes reproductive isolation among placental mammals (Eutheria). Topological comparison of <i>Zan</i> Maximum Likelihood phylogenies to a nearly complete mammalian supertree confirmed <i>Zan</i>’s striking phylogenetic utility and resolution at both deeper and more terminal nodes in the placental mammalian phylogeny. This single gene marker yielded an equivalent and/or superiorly supported topology in comparison to a supertree generated using DNA sequences from a supermatrix of 31 genes from 5911 species (extinct and extant). Resolution achieved with this new phylogenetic approach provides unique insights into the divergence of both early and recent mammalian radiations. Finally, and perhaps most importantly, the utility of zonadhesin as a singular molecular marker was especially useful in clades where sufficient taxon sampling is impossible to achieve, and where only a subset of members of the mammalian species tree is available. The eutherian relationships presented here provide a foundation for future studies in the reconstruction of mammalian classifications, including reproductive isolation, hybridization, and biodiversification of species.https://www.mdpi.com/1424-2818/15/11/1145molecular evolutionphylogeneticssupertreetanglegramzonadhesin
spellingShingle Emma K. Roberts
Emily A. Wright
Asha E. Worsham
Daniel M. Hardy
Robert D. Bradley
Gamete Recognition Gene Divergence Yields a Robust Eutherian Phylogeny across Taxonomic Levels
Diversity
molecular evolution
phylogenetics
supertree
tanglegram
zonadhesin
title Gamete Recognition Gene Divergence Yields a Robust Eutherian Phylogeny across Taxonomic Levels
title_full Gamete Recognition Gene Divergence Yields a Robust Eutherian Phylogeny across Taxonomic Levels
title_fullStr Gamete Recognition Gene Divergence Yields a Robust Eutherian Phylogeny across Taxonomic Levels
title_full_unstemmed Gamete Recognition Gene Divergence Yields a Robust Eutherian Phylogeny across Taxonomic Levels
title_short Gamete Recognition Gene Divergence Yields a Robust Eutherian Phylogeny across Taxonomic Levels
title_sort gamete recognition gene divergence yields a robust eutherian phylogeny across taxonomic levels
topic molecular evolution
phylogenetics
supertree
tanglegram
zonadhesin
url https://www.mdpi.com/1424-2818/15/11/1145
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