The unexpected genetic mating system of the red‐backed toadlet (Pseudophryne coriacea): A species with prolonged terrestrial breeding and cryptic reproductive behaviour
Molecular technologies have revolutionized our classification of animal mating systems, yet we still know very little about the genetic mating systems of many vertebrate groups. It is widely believed that anuran amphibians have the highest reproductive diversity of all vertebrates, yet genetic matin...
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Veröffentlicht in: | Molecular ecology 2018-07, Vol.27 (14), p.3001-3015 |
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creator | O'Brien, Daniel M. Keogh, J. Scott Silla, Aimee J. Byrne, Phillip G. |
description | Molecular technologies have revolutionized our classification of animal mating systems, yet we still know very little about the genetic mating systems of many vertebrate groups. It is widely believed that anuran amphibians have the highest reproductive diversity of all vertebrates, yet genetic mating systems have been studied in |
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Scott ; Silla, Aimee J. ; Byrne, Phillip G.</creator><creatorcontrib>O'Brien, Daniel M. ; Keogh, J. Scott ; Silla, Aimee J. ; Byrne, Phillip G.</creatorcontrib><description>Molecular technologies have revolutionized our classification of animal mating systems, yet we still know very little about the genetic mating systems of many vertebrate groups. It is widely believed that anuran amphibians have the highest reproductive diversity of all vertebrates, yet genetic mating systems have been studied in <1% of all described species. Here, we use single nucleotide polymorphisms to quantify the genetic mating system of the terrestrial breeding red‐backed toadlet Pseudophryne coriacea. In this species, breeding is prolonged (approximately 5 months), and males construct subterranean nests in which females deposit eggs. We predicted that females would display extreme sequential polyandry because this mating system has been reported in a closely related species (P. bibronii). Parentage analysis revealed that mating success was heavily skewed towards a subset of males (30.6% of potential sires) and that nearly all females (92.6%) mated with one male. In a high percentage of occupied nests (37.1%), the resident male was not the genetic sire, and very few nests (4.3%) contained clutches with multiple paternity. Unexpectedly, these results show that sequential polyandry is rare. They also show that there is a high frequency of nest takeover and extreme competition between males for nest sites, but that males rarely sneak matings. Genetic analysis also revealed introgressive hybridization between P. coriacea and the red‐crowned toadlet (Pseudophryne australis). Our study demonstrates a high level of mating system complexity, and it shows that closely related anurans can vary dramatically in their genetic mating system.</description><identifier>ISSN: 0962-1083</identifier><identifier>EISSN: 1365-294X</identifier><identifier>DOI: 10.1111/mec.14737</identifier><identifier>PMID: 29862607</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>amphibian ; Amphibians ; Animal behavior ; Animal reproduction ; Breeding ; cryptic breeding ; Eggs ; Females ; Genetic analysis ; genetic mating system ; Hybridization ; Males ; Mating ; Molecular chains ; nest takeover ; Nests ; Paternity ; Polyandry ; Pseudophryne coriacea ; Reproductive behavior ; reproductive behaviour ; Single-nucleotide polymorphism ; Species ; Terrestrial environments ; Underground construction ; Vertebrates</subject><ispartof>Molecular ecology, 2018-07, Vol.27 (14), p.3001-3015</ispartof><rights>2018 John Wiley & Sons Ltd</rights><rights>2018 John Wiley & Sons Ltd.</rights><rights>Copyright © 2018 John Wiley & Sons Ltd</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3887-9b543c339a529cea184b77f31e1d35e288daee410dba861dce1bf0e8919516853</citedby><cites>FETCH-LOGICAL-c3887-9b543c339a529cea184b77f31e1d35e288daee410dba861dce1bf0e8919516853</cites><orcidid>0000-0002-2277-9030 ; 0000-0003-2183-9959 ; 0000-0002-1373-6186 ; 0000-0003-2163-6254</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fmec.14737$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fmec.14737$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,27901,27902,45550,45551</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29862607$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>O'Brien, Daniel M.</creatorcontrib><creatorcontrib>Keogh, J. Scott</creatorcontrib><creatorcontrib>Silla, Aimee J.</creatorcontrib><creatorcontrib>Byrne, Phillip G.</creatorcontrib><title>The unexpected genetic mating system of the red‐backed toadlet (Pseudophryne coriacea): A species with prolonged terrestrial breeding and cryptic reproductive behaviour</title><title>Molecular ecology</title><addtitle>Mol Ecol</addtitle><description>Molecular technologies have revolutionized our classification of animal mating systems, yet we still know very little about the genetic mating systems of many vertebrate groups. It is widely believed that anuran amphibians have the highest reproductive diversity of all vertebrates, yet genetic mating systems have been studied in <1% of all described species. Here, we use single nucleotide polymorphisms to quantify the genetic mating system of the terrestrial breeding red‐backed toadlet Pseudophryne coriacea. In this species, breeding is prolonged (approximately 5 months), and males construct subterranean nests in which females deposit eggs. We predicted that females would display extreme sequential polyandry because this mating system has been reported in a closely related species (P. bibronii). Parentage analysis revealed that mating success was heavily skewed towards a subset of males (30.6% of potential sires) and that nearly all females (92.6%) mated with one male. In a high percentage of occupied nests (37.1%), the resident male was not the genetic sire, and very few nests (4.3%) contained clutches with multiple paternity. Unexpectedly, these results show that sequential polyandry is rare. They also show that there is a high frequency of nest takeover and extreme competition between males for nest sites, but that males rarely sneak matings. Genetic analysis also revealed introgressive hybridization between P. coriacea and the red‐crowned toadlet (Pseudophryne australis). Our study demonstrates a high level of mating system complexity, and it shows that closely related anurans can vary dramatically in their genetic mating system.</description><subject>amphibian</subject><subject>Amphibians</subject><subject>Animal behavior</subject><subject>Animal reproduction</subject><subject>Breeding</subject><subject>cryptic breeding</subject><subject>Eggs</subject><subject>Females</subject><subject>Genetic analysis</subject><subject>genetic mating system</subject><subject>Hybridization</subject><subject>Males</subject><subject>Mating</subject><subject>Molecular chains</subject><subject>nest takeover</subject><subject>Nests</subject><subject>Paternity</subject><subject>Polyandry</subject><subject>Pseudophryne coriacea</subject><subject>Reproductive behavior</subject><subject>reproductive behaviour</subject><subject>Single-nucleotide polymorphism</subject><subject>Species</subject><subject>Terrestrial environments</subject><subject>Underground construction</subject><subject>Vertebrates</subject><issn>0962-1083</issn><issn>1365-294X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><recordid>eNp10Utu1TAUBmALgeilMGADyBKTdpDWjzixmVVXpUVqBYMiMYsc--Rel7ywnbaZsQTW0WV1JTjc0gESnnjy-T-_fBB6S8kRTee4A3NE85KXz9CK8kJkTOXfnqMVUQXLKJF8D70K4ZoQypkQL9EeU7JgBSlX6P5qC3jq4W4EE8HiDfQQncGdjq7f4DCHCB0eGhyT82Affv6qtfmeZBy0bSHigy8BJjuMWz_3gM3gnTagDz_gExxSqIOAb13c4tEP7dBvlpfgPYSYYItrD2CXSbq32Ph5XIZ7SNhOJrobwDVs9Y0bJv8avWh0G-DN472Pvn48vVqfZxefzz6tTy4yw6UsM1WLnBvOlRZMpSZU5nVZNpwCtVwAk9JqgJwSW2tZUGuA1g0BqagStJCC76ODXW4q8WNKRavOBQNtq3sYplAxkiuVflnQRN__Q69T0T61S6qQTChJF3W4U8YPIXhoqtG7Tvu5oqRaFlilBVZ_Fpjsu8fEqe7APsm_G0vgeAduXQvz_5Oqy9P1LvI3QAWo9A</recordid><startdate>201807</startdate><enddate>201807</enddate><creator>O'Brien, Daniel M.</creator><creator>Keogh, J. 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Scott ; Silla, Aimee J. ; Byrne, Phillip G.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3887-9b543c339a529cea184b77f31e1d35e288daee410dba861dce1bf0e8919516853</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>amphibian</topic><topic>Amphibians</topic><topic>Animal behavior</topic><topic>Animal reproduction</topic><topic>Breeding</topic><topic>cryptic breeding</topic><topic>Eggs</topic><topic>Females</topic><topic>Genetic analysis</topic><topic>genetic mating system</topic><topic>Hybridization</topic><topic>Males</topic><topic>Mating</topic><topic>Molecular chains</topic><topic>nest takeover</topic><topic>Nests</topic><topic>Paternity</topic><topic>Polyandry</topic><topic>Pseudophryne coriacea</topic><topic>Reproductive behavior</topic><topic>reproductive behaviour</topic><topic>Single-nucleotide polymorphism</topic><topic>Species</topic><topic>Terrestrial environments</topic><topic>Underground construction</topic><topic>Vertebrates</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>O'Brien, Daniel M.</creatorcontrib><creatorcontrib>Keogh, J. Scott</creatorcontrib><creatorcontrib>Silla, Aimee J.</creatorcontrib><creatorcontrib>Byrne, Phillip G.</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Molecular ecology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>O'Brien, Daniel M.</au><au>Keogh, J. Scott</au><au>Silla, Aimee J.</au><au>Byrne, Phillip G.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The unexpected genetic mating system of the red‐backed toadlet (Pseudophryne coriacea): A species with prolonged terrestrial breeding and cryptic reproductive behaviour</atitle><jtitle>Molecular ecology</jtitle><addtitle>Mol Ecol</addtitle><date>2018-07</date><risdate>2018</risdate><volume>27</volume><issue>14</issue><spage>3001</spage><epage>3015</epage><pages>3001-3015</pages><issn>0962-1083</issn><eissn>1365-294X</eissn><abstract>Molecular technologies have revolutionized our classification of animal mating systems, yet we still know very little about the genetic mating systems of many vertebrate groups. It is widely believed that anuran amphibians have the highest reproductive diversity of all vertebrates, yet genetic mating systems have been studied in <1% of all described species. Here, we use single nucleotide polymorphisms to quantify the genetic mating system of the terrestrial breeding red‐backed toadlet Pseudophryne coriacea. In this species, breeding is prolonged (approximately 5 months), and males construct subterranean nests in which females deposit eggs. We predicted that females would display extreme sequential polyandry because this mating system has been reported in a closely related species (P. bibronii). Parentage analysis revealed that mating success was heavily skewed towards a subset of males (30.6% of potential sires) and that nearly all females (92.6%) mated with one male. In a high percentage of occupied nests (37.1%), the resident male was not the genetic sire, and very few nests (4.3%) contained clutches with multiple paternity. Unexpectedly, these results show that sequential polyandry is rare. They also show that there is a high frequency of nest takeover and extreme competition between males for nest sites, but that males rarely sneak matings. Genetic analysis also revealed introgressive hybridization between P. coriacea and the red‐crowned toadlet (Pseudophryne australis). Our study demonstrates a high level of mating system complexity, and it shows that closely related anurans can vary dramatically in their genetic mating system.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>29862607</pmid><doi>10.1111/mec.14737</doi><tpages>15</tpages><orcidid>https://orcid.org/0000-0002-2277-9030</orcidid><orcidid>https://orcid.org/0000-0003-2183-9959</orcidid><orcidid>https://orcid.org/0000-0002-1373-6186</orcidid><orcidid>https://orcid.org/0000-0003-2163-6254</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | amphibian Amphibians Animal behavior Animal reproduction Breeding cryptic breeding Eggs Females Genetic analysis genetic mating system Hybridization Males Mating Molecular chains nest takeover Nests Paternity Polyandry Pseudophryne coriacea Reproductive behavior reproductive behaviour Single-nucleotide polymorphism Species Terrestrial environments Underground construction Vertebrates |
title | The unexpected genetic mating system of the red‐backed toadlet (Pseudophryne coriacea): A species with prolonged terrestrial breeding and cryptic reproductive behaviour |
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