Evolution of salinity tolerance in the diving beetle tribe Hygrotini (Coleoptera, Dytiscidae)
Some species of the diving beetle tribe Hygrotini (subfamily Hydroporinae) are among the few insects able to tolerate saline concentrations more than twice that of seawater. However, the phylogenetic relationships of the species of Hygrotini, and the origin and evolution of tolerance to salinity in...
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description | Some species of the diving beetle tribe Hygrotini (subfamily Hydroporinae) are among the few insects able to tolerate saline concentrations more than twice that of seawater. However, the phylogenetic relationships of the species of Hygrotini, and the origin and evolution of tolerance to salinity in this lineage, are unknown. In this work, we aim to reconstruct how many times salinity tolerance did evolve in Hygrotini, whether this evolution was gradual or if tolerance to hypersalinity could evolve directly from strictly freshwater (FW) species, and to estimate the probabilities of transition between habitats. We build a phylogeny with ca. 45% of the 137 species of Hygrotini, including all major lineages and almost all of the known halophile or tolerant species. We used sequence data of four mitochondrial (COI‐5′, COI‐3′, 16S + tRNA and NADH1) and three nuclear (28S, 18S and H3) gene fragments, plus ecological data to reconstruct the history of the salinity tolerance using Bayesian inference. Our results demonstrate multiple origins of the tolerance to salinity, although most saline and hypersaline species were concentrated in two lineages. The evolution of salinity was gradual, with no direct transitions from FW to hypersaline habitats, but with some reversals from tolerant to FW species. The oldest transition to saline tolerance, at the base of the clade with the highest number of saline species, was dated in the late Eocene‐early Oligocene, a period with decreasing temperature and precipitation. This temporal coincidence suggests a link between increased aridity and the development of tolerance to saline waters, in agreement with recent research in other groups of aquatic Coleoptera. |
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However, the phylogenetic relationships of the species of Hygrotini, and the origin and evolution of tolerance to salinity in this lineage, are unknown. In this work, we aim to reconstruct how many times salinity tolerance did evolve in Hygrotini, whether this evolution was gradual or if tolerance to hypersalinity could evolve directly from strictly freshwater (FW) species, and to estimate the probabilities of transition between habitats. We build a phylogeny with ca. 45% of the 137 species of Hygrotini, including all major lineages and almost all of the known halophile or tolerant species. We used sequence data of four mitochondrial (COI‐5′, COI‐3′, 16S + tRNA and NADH1) and three nuclear (28S, 18S and H3) gene fragments, plus ecological data to reconstruct the history of the salinity tolerance using Bayesian inference. Our results demonstrate multiple origins of the tolerance to salinity, although most saline and hypersaline species were concentrated in two lineages. The evolution of salinity was gradual, with no direct transitions from FW to hypersaline habitats, but with some reversals from tolerant to FW species. The oldest transition to saline tolerance, at the base of the clade with the highest number of saline species, was dated in the late Eocene‐early Oligocene, a period with decreasing temperature and precipitation. This temporal coincidence suggests a link between increased aridity and the development of tolerance to saline waters, in agreement with recent research in other groups of aquatic Coleoptera.</description><identifier>ISSN: 0300-3256</identifier><identifier>EISSN: 1463-6409</identifier><identifier>DOI: 10.1111/zsc.12255</identifier><language>eng</language><publisher>Oslo: Wiley Subscription Services, Inc</publisher><subject>Animal biology ; Aquatic insects ; Aridity ; Bayesian analysis ; Biological evolution ; Coleoptera ; Diving ; Eocene ; Evolution ; Freshwater ; Hygrotini ; Inland water environment ; Insects ; Invertebrate Zoology ; Life Sciences ; Mitochondria ; Oligocene ; Phylogeny ; Probability theory ; Saline water ; Salinity ; Salinity effects ; Salinity tolerance ; Seawater ; Species ; Statistical inference ; tRNA</subject><ispartof>Zoologica scripta, 2018-01, Vol.47 (1), p.63-71</ispartof><rights>2017 Royal Swedish Academy of Sciences</rights><rights>Copyright © 2018 The Norwegian Academy of Science and Letters</rights><rights>Attribution</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3665-433257fbc9db14845bf91f36fc60d5e183f983b3ae34c3ae4e3094fef86902023</citedby><cites>FETCH-LOGICAL-c3665-433257fbc9db14845bf91f36fc60d5e183f983b3ae34c3ae4e3094fef86902023</cites><orcidid>0000-0002-2791-7615 ; 0000-0001-9728-5580</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%2Fzsc.12255$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fzsc.12255$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>230,315,781,785,886,1418,4025,27927,27928,27929,45578,45579</link.rule.ids><backlink>$$Uhttps://hal.sorbonne-universite.fr/hal-01744452$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Villastrigo, Adrián</creatorcontrib><creatorcontrib>Fery, Hans</creatorcontrib><creatorcontrib>Manuel, Michaël</creatorcontrib><creatorcontrib>Millán, Andrés</creatorcontrib><creatorcontrib>Ribera, Ignacio</creatorcontrib><title>Evolution of salinity tolerance in the diving beetle tribe Hygrotini (Coleoptera, Dytiscidae)</title><title>Zoologica scripta</title><description>Some species of the diving beetle tribe Hygrotini (subfamily Hydroporinae) are among the few insects able to tolerate saline concentrations more than twice that of seawater. However, the phylogenetic relationships of the species of Hygrotini, and the origin and evolution of tolerance to salinity in this lineage, are unknown. In this work, we aim to reconstruct how many times salinity tolerance did evolve in Hygrotini, whether this evolution was gradual or if tolerance to hypersalinity could evolve directly from strictly freshwater (FW) species, and to estimate the probabilities of transition between habitats. We build a phylogeny with ca. 45% of the 137 species of Hygrotini, including all major lineages and almost all of the known halophile or tolerant species. We used sequence data of four mitochondrial (COI‐5′, COI‐3′, 16S + tRNA and NADH1) and three nuclear (28S, 18S and H3) gene fragments, plus ecological data to reconstruct the history of the salinity tolerance using Bayesian inference. Our results demonstrate multiple origins of the tolerance to salinity, although most saline and hypersaline species were concentrated in two lineages. The evolution of salinity was gradual, with no direct transitions from FW to hypersaline habitats, but with some reversals from tolerant to FW species. The oldest transition to saline tolerance, at the base of the clade with the highest number of saline species, was dated in the late Eocene‐early Oligocene, a period with decreasing temperature and precipitation. This temporal coincidence suggests a link between increased aridity and the development of tolerance to saline waters, in agreement with recent research in other groups of aquatic Coleoptera.</description><subject>Animal biology</subject><subject>Aquatic insects</subject><subject>Aridity</subject><subject>Bayesian analysis</subject><subject>Biological evolution</subject><subject>Coleoptera</subject><subject>Diving</subject><subject>Eocene</subject><subject>Evolution</subject><subject>Freshwater</subject><subject>Hygrotini</subject><subject>Inland water environment</subject><subject>Insects</subject><subject>Invertebrate Zoology</subject><subject>Life Sciences</subject><subject>Mitochondria</subject><subject>Oligocene</subject><subject>Phylogeny</subject><subject>Probability theory</subject><subject>Saline water</subject><subject>Salinity</subject><subject>Salinity effects</subject><subject>Salinity tolerance</subject><subject>Seawater</subject><subject>Species</subject><subject>Statistical inference</subject><subject>tRNA</subject><issn>0300-3256</issn><issn>1463-6409</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><recordid>eNp1kFFLwzAUhYMoOKcP_oOALwp2S5o0ax9HnU4Y-KC-CBLSNNkyajOTbFJ_vZkVffI-3AuX7xwOB4BzjEY4zvjTyxFO0yw7AANMGUkYRcUhGCCCUELSjB2DE-_XCKGcYTQAr7OdbbbB2BZaDb1oTGtCB4NtlBOtVNC0MKwUrM3OtEtYKRUaBYMzlYLzbulsiAJ4WUbebkLUXMObLhgvTS3U1Sk40qLx6uznDsHz7eypnCeLh7v7crpIJGEsSyiJySa6kkVdYZrTrNIF1oRpyVCdKZwTXeSkIkIRKuOmiqCCaqVzVqAUpWQIrnrflWj4xpk34TpuheHz6YLvfwhPKKVZusORvejZjbPvW-UDX9uta2M8joscE4pxyv4cpbPeO6V_bTHi-6Z5bJp_Nx3Zcc9-mEZ1_4P85bHsFV9tZX6E</recordid><startdate>201801</startdate><enddate>201801</enddate><creator>Villastrigo, Adrián</creator><creator>Fery, Hans</creator><creator>Manuel, Michaël</creator><creator>Millán, Andrés</creator><creator>Ribera, Ignacio</creator><general>Wiley Subscription Services, Inc</general><general>Wiley</general><scope>AAYXX</scope><scope>CITATION</scope><scope>7QG</scope><scope>7SN</scope><scope>7SS</scope><scope>C1K</scope><scope>F1W</scope><scope>H95</scope><scope>L.G</scope><scope>1XC</scope><scope>VOOES</scope><orcidid>https://orcid.org/0000-0002-2791-7615</orcidid><orcidid>https://orcid.org/0000-0001-9728-5580</orcidid></search><sort><creationdate>201801</creationdate><title>Evolution of salinity tolerance in the diving beetle tribe Hygrotini (Coleoptera, Dytiscidae)</title><author>Villastrigo, Adrián ; Fery, Hans ; Manuel, Michaël ; Millán, Andrés ; Ribera, Ignacio</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3665-433257fbc9db14845bf91f36fc60d5e183f983b3ae34c3ae4e3094fef86902023</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>Animal biology</topic><topic>Aquatic insects</topic><topic>Aridity</topic><topic>Bayesian analysis</topic><topic>Biological evolution</topic><topic>Coleoptera</topic><topic>Diving</topic><topic>Eocene</topic><topic>Evolution</topic><topic>Freshwater</topic><topic>Hygrotini</topic><topic>Inland water environment</topic><topic>Insects</topic><topic>Invertebrate Zoology</topic><topic>Life Sciences</topic><topic>Mitochondria</topic><topic>Oligocene</topic><topic>Phylogeny</topic><topic>Probability theory</topic><topic>Saline water</topic><topic>Salinity</topic><topic>Salinity effects</topic><topic>Salinity tolerance</topic><topic>Seawater</topic><topic>Species</topic><topic>Statistical inference</topic><topic>tRNA</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Villastrigo, Adrián</creatorcontrib><creatorcontrib>Fery, Hans</creatorcontrib><creatorcontrib>Manuel, Michaël</creatorcontrib><creatorcontrib>Millán, Andrés</creatorcontrib><creatorcontrib>Ribera, Ignacio</creatorcontrib><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><jtitle>Zoologica scripta</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Villastrigo, Adrián</au><au>Fery, Hans</au><au>Manuel, Michaël</au><au>Millán, Andrés</au><au>Ribera, Ignacio</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Evolution of salinity tolerance in the diving beetle tribe Hygrotini (Coleoptera, Dytiscidae)</atitle><jtitle>Zoologica scripta</jtitle><date>2018-01</date><risdate>2018</risdate><volume>47</volume><issue>1</issue><spage>63</spage><epage>71</epage><pages>63-71</pages><issn>0300-3256</issn><eissn>1463-6409</eissn><abstract>Some species of the diving beetle tribe Hygrotini (subfamily Hydroporinae) are among the few insects able to tolerate saline concentrations more than twice that of seawater. However, the phylogenetic relationships of the species of Hygrotini, and the origin and evolution of tolerance to salinity in this lineage, are unknown. In this work, we aim to reconstruct how many times salinity tolerance did evolve in Hygrotini, whether this evolution was gradual or if tolerance to hypersalinity could evolve directly from strictly freshwater (FW) species, and to estimate the probabilities of transition between habitats. We build a phylogeny with ca. 45% of the 137 species of Hygrotini, including all major lineages and almost all of the known halophile or tolerant species. We used sequence data of four mitochondrial (COI‐5′, COI‐3′, 16S + tRNA and NADH1) and three nuclear (28S, 18S and H3) gene fragments, plus ecological data to reconstruct the history of the salinity tolerance using Bayesian inference. Our results demonstrate multiple origins of the tolerance to salinity, although most saline and hypersaline species were concentrated in two lineages. The evolution of salinity was gradual, with no direct transitions from FW to hypersaline habitats, but with some reversals from tolerant to FW species. The oldest transition to saline tolerance, at the base of the clade with the highest number of saline species, was dated in the late Eocene‐early Oligocene, a period with decreasing temperature and precipitation. This temporal coincidence suggests a link between increased aridity and the development of tolerance to saline waters, in agreement with recent research in other groups of aquatic Coleoptera.</abstract><cop>Oslo</cop><pub>Wiley Subscription Services, Inc</pub><doi>10.1111/zsc.12255</doi><tpages>9</tpages><orcidid>https://orcid.org/0000-0002-2791-7615</orcidid><orcidid>https://orcid.org/0000-0001-9728-5580</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Animal biology Aquatic insects Aridity Bayesian analysis Biological evolution Coleoptera Diving Eocene Evolution Freshwater Hygrotini Inland water environment Insects Invertebrate Zoology Life Sciences Mitochondria Oligocene Phylogeny Probability theory Saline water Salinity Salinity effects Salinity tolerance Seawater Species Statistical inference tRNA |
title | Evolution of salinity tolerance in the diving beetle tribe Hygrotini (Coleoptera, Dytiscidae) |
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