Adaptive radiation and speciation in Rhipicephalus ticks: A medley of novel hosts, nested predator-prey food webs, off-host periods and dispersal along temperature variation gradients
[Display omitted] •Rhipicephalus origin linked to host shifts between extinct predators and ungulates.•Dispersal out of Africa occurred in three lineages, and one dispersed back to Africa.•Temperature ranges and host-linked dispersal associated with diversification rates. Rhipicephalus are a species...
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Veröffentlicht in: | Molecular phylogenetics and evolution 2021-09, Vol.162, p.107178-107178, Article 107178 |
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creator | Bakkes, Deon K. Ropiquet, Anne Chitimia-Dobler, Lidia Matloa, Dikeledi E. Apanaskevich, Dmitry A. Horak, Ivan G. Mans, Ben J. Matthee, Conrad A. |
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•Rhipicephalus origin linked to host shifts between extinct predators and ungulates.•Dispersal out of Africa occurred in three lineages, and one dispersed back to Africa.•Temperature ranges and host-linked dispersal associated with diversification rates.
Rhipicephalus are a species-diverse genus of ticks, mainly distributed in the Afrotropics with some species in the Palearctic and Oriental regions. Current taxonomic consensus comprise nine informal species groups/lineages based on immature morphology. This work integrates biogeographic, ecological and molecular lines of evidence to better understand Rhipicephalus evolution. Phylogenetic analysis based on four genes (12S, 16S, 28S-D2 and COI) recovered five distinct clades with nine descendant clades that are generally congruent with current taxonomy, with some exceptions. Historical biogeography is inferred from molecular divergence times, ancestral distribution areas, host-use and climate niches of four phylogenetically significant bioclimatic variables (isothermality, annual, seasonal and diurnal temperature range). Novel hosts enabled host-linked dispersal events into new environments, and ticks exploited new hosts through nested predator-prey connections in food webs. Diversification was further induced by climate niche partitioning along gradients in temperature range during off-host periods. Ancestral climate niche estimates corroborated dispersal events by indicating hypothetical ancestors moved into environments with different annual and seasonal temperature ranges along latitudinal gradients. Host size for immature and adult life stages was important for dispersal and subsequent diversification rates. Clades that utilise large, mobile hosts (ungulates and carnivores) early in development have wider geographic ranges but slower diversification rates, and those utilising small, less mobile hosts (rodents, lagomorphs and afroinsectivores) early in development have smaller ranges but higher diversification rates. These findings suggest diversification is driven by a complex set of factors linked to both host-associations (host size, ranges and mobility) and climate niche partitioning along annual and seasonal temperature range gradients that vary with latitude. Moreover, competitive interactions can reinforce these processes and drive speciation. Off-host periods facilitate adaptive radiation by enabling host switches along nested predator-prey connections in food webs, but at the c |
doi_str_mv | 10.1016/j.ympev.2021.107178 |
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•Rhipicephalus origin linked to host shifts between extinct predators and ungulates.•Dispersal out of Africa occurred in three lineages, and one dispersed back to Africa.•Temperature ranges and host-linked dispersal associated with diversification rates.
Rhipicephalus are a species-diverse genus of ticks, mainly distributed in the Afrotropics with some species in the Palearctic and Oriental regions. Current taxonomic consensus comprise nine informal species groups/lineages based on immature morphology. This work integrates biogeographic, ecological and molecular lines of evidence to better understand Rhipicephalus evolution. Phylogenetic analysis based on four genes (12S, 16S, 28S-D2 and COI) recovered five distinct clades with nine descendant clades that are generally congruent with current taxonomy, with some exceptions. Historical biogeography is inferred from molecular divergence times, ancestral distribution areas, host-use and climate niches of four phylogenetically significant bioclimatic variables (isothermality, annual, seasonal and diurnal temperature range). Novel hosts enabled host-linked dispersal events into new environments, and ticks exploited new hosts through nested predator-prey connections in food webs. Diversification was further induced by climate niche partitioning along gradients in temperature range during off-host periods. Ancestral climate niche estimates corroborated dispersal events by indicating hypothetical ancestors moved into environments with different annual and seasonal temperature ranges along latitudinal gradients. Host size for immature and adult life stages was important for dispersal and subsequent diversification rates. Clades that utilise large, mobile hosts (ungulates and carnivores) early in development have wider geographic ranges but slower diversification rates, and those utilising small, less mobile hosts (rodents, lagomorphs and afroinsectivores) early in development have smaller ranges but higher diversification rates. These findings suggest diversification is driven by a complex set of factors linked to both host-associations (host size, ranges and mobility) and climate niche partitioning along annual and seasonal temperature range gradients that vary with latitude. Moreover, competitive interactions can reinforce these processes and drive speciation. Off-host periods facilitate adaptive radiation by enabling host switches along nested predator-prey connections in food webs, but at the cost of environmental exposure that partitions niches among dispersing progenitors, disrupting geneflow and driving diversification. As such, the evolution and ecological niches of Rhipicephalus are characterised by trade-offs between on- and off-host periods, and these trade-offs interact with nested predator-prey connections in food webs, host-use at different life stages, as well as gradients in annual and seasonal temperature ranges to drive adaptive radiation and speciation.</description><identifier>ISSN: 1055-7903</identifier><identifier>EISSN: 1095-9513</identifier><identifier>DOI: 10.1016/j.ympev.2021.107178</identifier><identifier>PMID: 33892098</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Afrotropical ; Climate Niche ; Ectoparasite ; Host ; Phylogeny ; Tick</subject><ispartof>Molecular phylogenetics and evolution, 2021-09, Vol.162, p.107178-107178, Article 107178</ispartof><rights>2021 Elsevier Inc.</rights><rights>Copyright © 2021 Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c425t-54f352aae5ee757ae475185f2fc085f8150421019434ee8d8c431a58bee0154a3</citedby><cites>FETCH-LOGICAL-c425t-54f352aae5ee757ae475185f2fc085f8150421019434ee8d8c431a58bee0154a3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.ympev.2021.107178$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,780,784,3550,27924,27925,45995</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33892098$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Bakkes, Deon K.</creatorcontrib><creatorcontrib>Ropiquet, Anne</creatorcontrib><creatorcontrib>Chitimia-Dobler, Lidia</creatorcontrib><creatorcontrib>Matloa, Dikeledi E.</creatorcontrib><creatorcontrib>Apanaskevich, Dmitry A.</creatorcontrib><creatorcontrib>Horak, Ivan G.</creatorcontrib><creatorcontrib>Mans, Ben J.</creatorcontrib><creatorcontrib>Matthee, Conrad A.</creatorcontrib><title>Adaptive radiation and speciation in Rhipicephalus ticks: A medley of novel hosts, nested predator-prey food webs, off-host periods and dispersal along temperature variation gradients</title><title>Molecular phylogenetics and evolution</title><addtitle>Mol Phylogenet Evol</addtitle><description>[Display omitted]
•Rhipicephalus origin linked to host shifts between extinct predators and ungulates.•Dispersal out of Africa occurred in three lineages, and one dispersed back to Africa.•Temperature ranges and host-linked dispersal associated with diversification rates.
Rhipicephalus are a species-diverse genus of ticks, mainly distributed in the Afrotropics with some species in the Palearctic and Oriental regions. Current taxonomic consensus comprise nine informal species groups/lineages based on immature morphology. This work integrates biogeographic, ecological and molecular lines of evidence to better understand Rhipicephalus evolution. Phylogenetic analysis based on four genes (12S, 16S, 28S-D2 and COI) recovered five distinct clades with nine descendant clades that are generally congruent with current taxonomy, with some exceptions. Historical biogeography is inferred from molecular divergence times, ancestral distribution areas, host-use and climate niches of four phylogenetically significant bioclimatic variables (isothermality, annual, seasonal and diurnal temperature range). Novel hosts enabled host-linked dispersal events into new environments, and ticks exploited new hosts through nested predator-prey connections in food webs. Diversification was further induced by climate niche partitioning along gradients in temperature range during off-host periods. Ancestral climate niche estimates corroborated dispersal events by indicating hypothetical ancestors moved into environments with different annual and seasonal temperature ranges along latitudinal gradients. Host size for immature and adult life stages was important for dispersal and subsequent diversification rates. Clades that utilise large, mobile hosts (ungulates and carnivores) early in development have wider geographic ranges but slower diversification rates, and those utilising small, less mobile hosts (rodents, lagomorphs and afroinsectivores) early in development have smaller ranges but higher diversification rates. These findings suggest diversification is driven by a complex set of factors linked to both host-associations (host size, ranges and mobility) and climate niche partitioning along annual and seasonal temperature range gradients that vary with latitude. Moreover, competitive interactions can reinforce these processes and drive speciation. Off-host periods facilitate adaptive radiation by enabling host switches along nested predator-prey connections in food webs, but at the cost of environmental exposure that partitions niches among dispersing progenitors, disrupting geneflow and driving diversification. As such, the evolution and ecological niches of Rhipicephalus are characterised by trade-offs between on- and off-host periods, and these trade-offs interact with nested predator-prey connections in food webs, host-use at different life stages, as well as gradients in annual and seasonal temperature ranges to drive adaptive radiation and speciation.</description><subject>Afrotropical</subject><subject>Climate Niche</subject><subject>Ectoparasite</subject><subject>Host</subject><subject>Phylogeny</subject><subject>Tick</subject><issn>1055-7903</issn><issn>1095-9513</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><recordid>eNp9UctuFDEQHCEi8oAvQEI-cmA2fjIeJA6riABSJKQonC2v3c56mR0b2zNov4zfw5NdOHLqdru6q6uraV4TvCKYvL_erQ77CPOKYkpqpSOdfNZcENyLtheEPV9yIdqux-y8ucx5hzEhohcvmnPGZE9xLy-a32urY_EzoKSt18WHEenRohzBnJ5-RPdbH72BuNXDlFHx5kf-gNZoD3aAAwoOjWGGAW1DLvkdGiEXsCgmsLqE1NbkgFwIFv2CTf0PzrULFEVIPtj8RGh9pUxZD0gPYXxEBaq4pMuUAM06nXZ5XLaEseSXzZnTQ4ZXp3jVfL_99HDzpb379vnrzfquNZyK0grumKBagwDoRKeBd4JI4agzuAZJBOa0XrPnjANIKw1nRAu5AcBEcM2umrfHuTGFn1MVpvY-GxgGPUKYsqJ1HKVUSF6h7Ag1KeScwKmY_F6ngyJYLY6pnXpyTC2OqaNjtevNiWDa1Hv-6_lrUQV8PAKgypw9JJVNPYEB6xOYomzw_yX4A5XNrGk</recordid><startdate>20210901</startdate><enddate>20210901</enddate><creator>Bakkes, Deon K.</creator><creator>Ropiquet, Anne</creator><creator>Chitimia-Dobler, Lidia</creator><creator>Matloa, Dikeledi E.</creator><creator>Apanaskevich, Dmitry A.</creator><creator>Horak, Ivan G.</creator><creator>Mans, Ben J.</creator><creator>Matthee, Conrad A.</creator><general>Elsevier Inc</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope></search><sort><creationdate>20210901</creationdate><title>Adaptive radiation and speciation in Rhipicephalus ticks: A medley of novel hosts, nested predator-prey food webs, off-host periods and dispersal along temperature variation gradients</title><author>Bakkes, Deon K. ; Ropiquet, Anne ; Chitimia-Dobler, Lidia ; Matloa, Dikeledi E. ; Apanaskevich, Dmitry A. ; Horak, Ivan G. ; Mans, Ben J. ; Matthee, Conrad A.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c425t-54f352aae5ee757ae475185f2fc085f8150421019434ee8d8c431a58bee0154a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Afrotropical</topic><topic>Climate Niche</topic><topic>Ectoparasite</topic><topic>Host</topic><topic>Phylogeny</topic><topic>Tick</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Bakkes, Deon K.</creatorcontrib><creatorcontrib>Ropiquet, Anne</creatorcontrib><creatorcontrib>Chitimia-Dobler, Lidia</creatorcontrib><creatorcontrib>Matloa, Dikeledi E.</creatorcontrib><creatorcontrib>Apanaskevich, Dmitry A.</creatorcontrib><creatorcontrib>Horak, Ivan G.</creatorcontrib><creatorcontrib>Mans, Ben J.</creatorcontrib><creatorcontrib>Matthee, Conrad A.</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Molecular phylogenetics and evolution</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Bakkes, Deon K.</au><au>Ropiquet, Anne</au><au>Chitimia-Dobler, Lidia</au><au>Matloa, Dikeledi E.</au><au>Apanaskevich, Dmitry A.</au><au>Horak, Ivan G.</au><au>Mans, Ben J.</au><au>Matthee, Conrad A.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Adaptive radiation and speciation in Rhipicephalus ticks: A medley of novel hosts, nested predator-prey food webs, off-host periods and dispersal along temperature variation gradients</atitle><jtitle>Molecular phylogenetics and evolution</jtitle><addtitle>Mol Phylogenet Evol</addtitle><date>2021-09-01</date><risdate>2021</risdate><volume>162</volume><spage>107178</spage><epage>107178</epage><pages>107178-107178</pages><artnum>107178</artnum><issn>1055-7903</issn><eissn>1095-9513</eissn><abstract>[Display omitted]
•Rhipicephalus origin linked to host shifts between extinct predators and ungulates.•Dispersal out of Africa occurred in three lineages, and one dispersed back to Africa.•Temperature ranges and host-linked dispersal associated with diversification rates.
Rhipicephalus are a species-diverse genus of ticks, mainly distributed in the Afrotropics with some species in the Palearctic and Oriental regions. Current taxonomic consensus comprise nine informal species groups/lineages based on immature morphology. This work integrates biogeographic, ecological and molecular lines of evidence to better understand Rhipicephalus evolution. Phylogenetic analysis based on four genes (12S, 16S, 28S-D2 and COI) recovered five distinct clades with nine descendant clades that are generally congruent with current taxonomy, with some exceptions. Historical biogeography is inferred from molecular divergence times, ancestral distribution areas, host-use and climate niches of four phylogenetically significant bioclimatic variables (isothermality, annual, seasonal and diurnal temperature range). Novel hosts enabled host-linked dispersal events into new environments, and ticks exploited new hosts through nested predator-prey connections in food webs. Diversification was further induced by climate niche partitioning along gradients in temperature range during off-host periods. Ancestral climate niche estimates corroborated dispersal events by indicating hypothetical ancestors moved into environments with different annual and seasonal temperature ranges along latitudinal gradients. Host size for immature and adult life stages was important for dispersal and subsequent diversification rates. Clades that utilise large, mobile hosts (ungulates and carnivores) early in development have wider geographic ranges but slower diversification rates, and those utilising small, less mobile hosts (rodents, lagomorphs and afroinsectivores) early in development have smaller ranges but higher diversification rates. These findings suggest diversification is driven by a complex set of factors linked to both host-associations (host size, ranges and mobility) and climate niche partitioning along annual and seasonal temperature range gradients that vary with latitude. Moreover, competitive interactions can reinforce these processes and drive speciation. Off-host periods facilitate adaptive radiation by enabling host switches along nested predator-prey connections in food webs, but at the cost of environmental exposure that partitions niches among dispersing progenitors, disrupting geneflow and driving diversification. As such, the evolution and ecological niches of Rhipicephalus are characterised by trade-offs between on- and off-host periods, and these trade-offs interact with nested predator-prey connections in food webs, host-use at different life stages, as well as gradients in annual and seasonal temperature ranges to drive adaptive radiation and speciation.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>33892098</pmid><doi>10.1016/j.ympev.2021.107178</doi><tpages>1</tpages></addata></record> |
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subjects | Afrotropical Climate Niche Ectoparasite Host Phylogeny Tick |
title | Adaptive radiation and speciation in Rhipicephalus ticks: A medley of novel hosts, nested predator-prey food webs, off-host periods and dispersal along temperature variation gradients |
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