How common is ecological speciation in plant-feeding insects? A 'Higher' Nematinae perspective
Identifieur interne : 000489 ( Pmc/Curation ); précédent : 000488; suivant : 000490How common is ecological speciation in plant-feeding insects? A 'Higher' Nematinae perspective
Auteurs : Tommi Nyman [Finlande] ; Veli Vikberg [Finlande] ; David R. Smith [États-Unis] ; Jean-Luc Boevé [Belgique]Source :
- BMC Evolutionary Biology [ 1471-2148 ] ; 2010.
Abstract
Ecological speciation is a process in which a transiently resource-polymorphic species divides into two specialized sister lineages as a result of divergent selection pressures caused by the use of multiple niches or environments. Ecology-based speciation has been studied intensively in plant-feeding insects, in which both sympatric and allopatric shifts onto novel host plants could speed up diversification. However, while numerous examples of species pairs likely to have originated by resource shifts have been found, the overall importance of ecological speciation in relation to other, non-ecological speciation modes remains unknown. Here, we apply phylogenetic information on sawflies belonging to the 'Higher' Nematinae (Hymenoptera: Tenthredinidae) to infer the frequency of niche shifts in relation to speciation events.
Phylogenetic trees reconstructed on the basis of DNA sequence data show that the diversification of higher nematines has involved frequent shifts in larval feeding habits and in the use of plant taxa. However, the inferred number of resource shifts is considerably lower than the number of past speciation events, indicating that the majority of divergences have occurred by non-ecological allopatric speciation; based on a time-corrected analysis of sister species, we estimate that a maximum of
Our analysis indicates that the importance of niche shifts for the diversification of herbivorous insects is at present implicitly and explicitly overestimated. In the case of the Higher Nematinae, employing a time correction for sister-species comparisons lowered the proportion of apparent ecology-based speciation events from
Url:
DOI: 10.1186/1471-2148-10-266
PubMed: 20807452
PubMed Central: 2936908
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<author><name sortKey="Nyman, Tommi" sort="Nyman, Tommi" uniqKey="Nyman T" first="Tommi" last="Nyman">Tommi Nyman</name>
<affiliation wicri:level="1"><nlm:aff id="I1">Department of Biology, University of Eastern Finland, P.O. Box 111, FI-80101 Joensuu, Finland</nlm:aff>
<country xml:lang="fr">Finlande</country>
<wicri:regionArea>Department of Biology, University of Eastern Finland, P.O. Box 111, FI-80101 Joensuu</wicri:regionArea>
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<author><name sortKey="Vikberg, Veli" sort="Vikberg, Veli" uniqKey="Vikberg V" first="Veli" last="Vikberg">Veli Vikberg</name>
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<author><name sortKey="Smith, David R" sort="Smith, David R" uniqKey="Smith D" first="David R" last="Smith">David R. Smith</name>
<affiliation wicri:level="1"><nlm:aff id="I3">Systematic Entomology Laboratory, PSI, Agricultural Research Service, US Department of Agriculture, c/o National Museum of Natural History, Smithsonian Institution, P.O. Box 37012, MRC 168, Washington, DC 20013-7012, USA</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Systematic Entomology Laboratory, PSI, Agricultural Research Service, US Department of Agriculture, c/o National Museum of Natural History, Smithsonian Institution, P.O. Box 37012, MRC 168, Washington, DC 20013-7012</wicri:regionArea>
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<author><name sortKey="Boeve, Jean Luc" sort="Boeve, Jean Luc" uniqKey="Boeve J" first="Jean-Luc" last="Boevé">Jean-Luc Boevé</name>
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<wicri:regionArea>Department of Entomology, Royal Belgian Institute of Natural Sciences, Rue Vautier 29, B-1000 Brussels</wicri:regionArea>
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">How common is ecological speciation in plant-feeding insects? A 'Higher' Nematinae perspective</title>
<author><name sortKey="Nyman, Tommi" sort="Nyman, Tommi" uniqKey="Nyman T" first="Tommi" last="Nyman">Tommi Nyman</name>
<affiliation wicri:level="1"><nlm:aff id="I1">Department of Biology, University of Eastern Finland, P.O. Box 111, FI-80101 Joensuu, Finland</nlm:aff>
<country xml:lang="fr">Finlande</country>
<wicri:regionArea>Department of Biology, University of Eastern Finland, P.O. Box 111, FI-80101 Joensuu</wicri:regionArea>
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<author><name sortKey="Vikberg, Veli" sort="Vikberg, Veli" uniqKey="Vikberg V" first="Veli" last="Vikberg">Veli Vikberg</name>
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<author><name sortKey="Smith, David R" sort="Smith, David R" uniqKey="Smith D" first="David R" last="Smith">David R. Smith</name>
<affiliation wicri:level="1"><nlm:aff id="I3">Systematic Entomology Laboratory, PSI, Agricultural Research Service, US Department of Agriculture, c/o National Museum of Natural History, Smithsonian Institution, P.O. Box 37012, MRC 168, Washington, DC 20013-7012, USA</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Systematic Entomology Laboratory, PSI, Agricultural Research Service, US Department of Agriculture, c/o National Museum of Natural History, Smithsonian Institution, P.O. Box 37012, MRC 168, Washington, DC 20013-7012</wicri:regionArea>
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<author><name sortKey="Boeve, Jean Luc" sort="Boeve, Jean Luc" uniqKey="Boeve J" first="Jean-Luc" last="Boevé">Jean-Luc Boevé</name>
<affiliation wicri:level="1"><nlm:aff id="I4">Department of Entomology, Royal Belgian Institute of Natural Sciences, Rue Vautier 29, B-1000 Brussels, Belgium</nlm:aff>
<country xml:lang="fr">Belgique</country>
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<series><title level="j">BMC Evolutionary Biology</title>
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<front><div type="abstract" xml:lang="en"><sec><title>Background</title>
<p>Ecological speciation is a process in which a transiently resource-polymorphic species divides into two specialized sister lineages as a result of divergent selection pressures caused by the use of multiple niches or environments. Ecology-based speciation has been studied intensively in plant-feeding insects, in which both sympatric and allopatric shifts onto novel host plants could speed up diversification. However, while numerous examples of species pairs likely to have originated by resource shifts have been found, the overall importance of ecological speciation in relation to other, non-ecological speciation modes remains unknown. Here, we apply phylogenetic information on sawflies belonging to the 'Higher' Nematinae (Hymenoptera: Tenthredinidae) to infer the frequency of niche shifts in relation to speciation events.</p>
</sec>
<sec><title>Results</title>
<p>Phylogenetic trees reconstructed on the basis of DNA sequence data show that the diversification of higher nematines has involved frequent shifts in larval feeding habits and in the use of plant taxa. However, the inferred number of resource shifts is considerably lower than the number of past speciation events, indicating that the majority of divergences have occurred by non-ecological allopatric speciation; based on a time-corrected analysis of sister species, we estimate that a maximum of <italic>c</italic>
. 20% of lineage splits have been triggered by a change in resource use. In addition, we find that postspeciational changes in geographic distributions have led to broad sympatry in many species having identical host-plant ranges.</p>
</sec>
<sec><title>Conclusion</title>
<p>Our analysis indicates that the importance of niche shifts for the diversification of herbivorous insects is at present implicitly and explicitly overestimated. In the case of the Higher Nematinae, employing a time correction for sister-species comparisons lowered the proportion of apparent ecology-based speciation events from <italic>c</italic>
. 50-60% to around 20%, but such corrections are still lacking in other herbivore groups. The observed convergent but asynchronous shifting among dominant northern plant taxa in many higher-nematine clades, in combination with the broad overlaps in the geographic distributions of numerous nematine species occupying near-identical niches, indicates that host-plant shifts and herbivore community assembly are largely unconstrained by direct or indirect competition among species. More phylogeny-based studies on connections between niche diversification and speciation are needed across many insect taxa, especially in groups that exhibit few host shifts in relation to speciation.</p>
</sec>
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<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">BMC Evol Biol</journal-id>
<journal-title-group><journal-title>BMC Evolutionary Biology</journal-title>
</journal-title-group>
<issn pub-type="epub">1471-2148</issn>
<publisher><publisher-name>BioMed Central</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">20807452</article-id>
<article-id pub-id-type="pmc">2936908</article-id>
<article-id pub-id-type="publisher-id">1471-2148-10-266</article-id>
<article-id pub-id-type="doi">10.1186/1471-2148-10-266</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject>
</subj-group>
</article-categories>
<title-group><article-title>How common is ecological speciation in plant-feeding insects? A 'Higher' Nematinae perspective</article-title>
</title-group>
<contrib-group><contrib contrib-type="author" corresp="yes" id="A1"><name><surname>Nyman</surname>
<given-names>Tommi</given-names>
</name>
<xref ref-type="aff" rid="I1">1</xref>
<email>Tommi.Nyman@uef.fi</email>
</contrib>
<contrib contrib-type="author" id="A2"><name><surname>Vikberg</surname>
<given-names>Veli</given-names>
</name>
<xref ref-type="aff" rid="I2">2</xref>
<email>Veli.Vikberg@aina.net</email>
</contrib>
<contrib contrib-type="author" id="A3"><name><surname>Smith</surname>
<given-names>David R</given-names>
</name>
<xref ref-type="aff" rid="I3">3</xref>
<email>Dave.Smith@ars.usda.gov</email>
</contrib>
<contrib contrib-type="author" id="A4"><name><surname>Boevé</surname>
<given-names>Jean-Luc</given-names>
</name>
<xref ref-type="aff" rid="I4">4</xref>
<email>Jean-Luc.Boeve@naturalsciences.be</email>
</contrib>
</contrib-group>
<aff id="I1"><label>1</label>
Department of Biology, University of Eastern Finland, P.O. Box 111, FI-80101 Joensuu, Finland</aff>
<aff id="I2"><label>2</label>
Liinalammintie 11 as. 6, FI-14200 Turenki, Finland</aff>
<aff id="I3"><label>3</label>
Systematic Entomology Laboratory, PSI, Agricultural Research Service, US Department of Agriculture, c/o National Museum of Natural History, Smithsonian Institution, P.O. Box 37012, MRC 168, Washington, DC 20013-7012, USA</aff>
<aff id="I4"><label>4</label>
Department of Entomology, Royal Belgian Institute of Natural Sciences, Rue Vautier 29, B-1000 Brussels, Belgium</aff>
<pub-date pub-type="collection"><year>2010</year>
</pub-date>
<pub-date pub-type="epub"><day>1</day>
<month>9</month>
<year>2010</year>
</pub-date>
<volume>10</volume>
<fpage>266</fpage>
<lpage>266</lpage>
<history><date date-type="received"><day>14</day>
<month>2</month>
<year>2010</year>
</date>
<date date-type="accepted"><day>1</day>
<month>9</month>
<year>2010</year>
</date>
</history>
<permissions><copyright-statement>Copyright ©2010 Nyman et al; licensee BioMed Central Ltd.</copyright-statement>
<copyright-year>2010</copyright-year>
<copyright-holder>Nyman et al; licensee BioMed Central Ltd.</copyright-holder>
<license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by/2.0"><license-p>This is an Open Access article distributed under the terms of the Creative Commons Attribution License (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/2.0">http://creativecommons.org/licenses/by/2.0</ext-link>
), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.</license-p>
</license>
</permissions>
<self-uri xlink:href="http://www.biomedcentral.com/1471-2148/10/266"></self-uri>
<abstract><sec><title>Background</title>
<p>Ecological speciation is a process in which a transiently resource-polymorphic species divides into two specialized sister lineages as a result of divergent selection pressures caused by the use of multiple niches or environments. Ecology-based speciation has been studied intensively in plant-feeding insects, in which both sympatric and allopatric shifts onto novel host plants could speed up diversification. However, while numerous examples of species pairs likely to have originated by resource shifts have been found, the overall importance of ecological speciation in relation to other, non-ecological speciation modes remains unknown. Here, we apply phylogenetic information on sawflies belonging to the 'Higher' Nematinae (Hymenoptera: Tenthredinidae) to infer the frequency of niche shifts in relation to speciation events.</p>
</sec>
<sec><title>Results</title>
<p>Phylogenetic trees reconstructed on the basis of DNA sequence data show that the diversification of higher nematines has involved frequent shifts in larval feeding habits and in the use of plant taxa. However, the inferred number of resource shifts is considerably lower than the number of past speciation events, indicating that the majority of divergences have occurred by non-ecological allopatric speciation; based on a time-corrected analysis of sister species, we estimate that a maximum of <italic>c</italic>
. 20% of lineage splits have been triggered by a change in resource use. In addition, we find that postspeciational changes in geographic distributions have led to broad sympatry in many species having identical host-plant ranges.</p>
</sec>
<sec><title>Conclusion</title>
<p>Our analysis indicates that the importance of niche shifts for the diversification of herbivorous insects is at present implicitly and explicitly overestimated. In the case of the Higher Nematinae, employing a time correction for sister-species comparisons lowered the proportion of apparent ecology-based speciation events from <italic>c</italic>
. 50-60% to around 20%, but such corrections are still lacking in other herbivore groups. The observed convergent but asynchronous shifting among dominant northern plant taxa in many higher-nematine clades, in combination with the broad overlaps in the geographic distributions of numerous nematine species occupying near-identical niches, indicates that host-plant shifts and herbivore community assembly are largely unconstrained by direct or indirect competition among species. More phylogeny-based studies on connections between niche diversification and speciation are needed across many insect taxa, especially in groups that exhibit few host shifts in relation to speciation.</p>
</sec>
</abstract>
</article-meta>
</front>
</pmc>
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