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Neither philopatric nor panmictic: microsatellite and mtDNA evidence suggests lack of natal homing but limits to dispersal in Pacific lamprey

Identifieur interne : 001238 ( Istex/Corpus ); précédent : 001237; suivant : 001239

Neither philopatric nor panmictic: microsatellite and mtDNA evidence suggests lack of natal homing but limits to dispersal in Pacific lamprey

Auteurs : Erin K. Spice ; Damon H. Goodman ; Stewart B. Reid ; Margaret F. Docker

Source :

RBID : ISTEX:48918E62DF873F53D92128F443136EBCB4A3168D

English descriptors

Abstract

Most species with lengthy migrations display some degree of natal homing; some (e.g. migratory birds and anadromous salmonids) show spectacular feats of homing. However, studies of the sea lamprey (Petromyzon marinus) indicate that this anadromous species locates spawning habitat based on pheromonal cues from larvae rather than through philopatry. Previous genetic studies in the anadromous Pacific lamprey (Entosphenus tridentatus) have both supported and rejected the hypothesis of natal homing. To resolve this, we used nine microsatellite loci to examine the population structure in 965 Pacific lamprey from 20 locations from central British Columbia to southern California and supplemented this analysis with mitochondrial DNA restriction fragment length polymorphism analysis on a subset of 530 lamprey. Microsatellite analysis revealed (i) relatively low but often statistically significant genetic differentiation among locations (97% pairwise FST values were <0.04 but 73.7% were significant); and (ii) weak but significant isolation by distance (r2 = 0.0565, P = 0.0450) but no geographic clustering of samples. The few moderate FST values involved comparisons with sites that were geographically distant or far upstream. The mtDNA analysis—although providing less resolution among sites (only 4.7%FST values were significant)—was broadly consistent with the microsatellite results: (i) the southernmost site and some sites tributary to the Salish Sea were genetically distinct; and (ii) southern sites showed higher haplotype and private haplotype richness. These results are inconsistent with philopatry, suggesting that anadromous lampreys are unusual among species with long migrations, but suggest that limited dispersal at sea precludes panmixia in this species.

Url:
DOI: 10.1111/j.1365-294X.2012.05585.x

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ISTEX:48918E62DF873F53D92128F443136EBCB4A3168D

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</affiliation>
<affiliation xml:id="a3" countryCode="US">
<unparsedAffiliation>Western Fishes, 2045 East Main Street, Ashland, OR 97520, USA</unparsedAffiliation>
</affiliation>
</affiliationGroup>
<keywordGroup xml:lang="en">
<keyword xml:id="k1">anadromy</keyword>
<keyword xml:id="k2">
<i>Entosphenus</i>
</keyword>
<keyword xml:id="k3">microsatellite</keyword>
<keyword xml:id="k4">Pacific lamprey</keyword>
<keyword xml:id="k5">philopatry</keyword>
<keyword xml:id="k6">population structure</keyword>
</keywordGroup>
<supportingInformation>
<p>
<b>Table S1</b>
Summary statistics for each locus in Pacific lamprey (
<i>Entosphenus tridentatus</i>
) collected at 20 sites along the west coast of North America.
<b>Table S2</b>
Comparison of pairwise
<i>F</i>
<sub>ST</sub>
values generated from original (above the diagonal) and null allele corrected (below the diagonal) data, for Pacific lamprey (
<i>Entosphenus tridentatus</i>
) collected at 20 sites along the west coast of North America.
<b>Table S3</b>
Global
<i>F</i>
<sub>ST</sub>
(g
<i>F</i>
<sub>ST</sub>
) per locus estimated with and without the ENA correction described in Chapuis & Estoup (2007).
<b>Table S4</b>
Comparison of pairwise
<i>F</i>
<sub>ST</sub>
values calculated using GENEPOP v. 4.0.10 (Raymond & Rousset 1995; Rousset 2008) both with (above diagonal) and without (below diagonal) loci Etr‐2, Etr‐3, and Lri‐3 for Pacific lamprey (
<i>Entosphenus tridentatus</i>
) collected at 20 sites along the west coast of North America.
<b>Table S5</b>
Results of Colony (Jones & Wang 2010) sibship analysis for Pacific lamprey (
<i>Entosphenus tridentatus</i>
) collected at 20 sites along the west coast of North America.
<b>Table S6</b>
Jost’s
<i>D</i>
values calculated using SMOGD v.1.2.5 (Crawford 2010) for Pacific lamprey (
<i>Entosphenus tridentatus</i>
) collected at 20 sites along the west coast of North America.
<b>Table S7</b>
Restriction fragment length polymorphism (RFLP) composite haplotype frequencies for Pacific lamprey (
<i>Entosphenus tridentatus</i>
) collected at 20 sites along the west coast of North America, following Goodman
<i>et al.</i>
(2008); haplotype richness and private haplotype richness were calculated using rarefaction implemented in HP‐Rare (Kalinowski 2005).
<b>Fig. S1</b>
Neighbor‐joining trees produced with: (a) original data set using POPULATIONS v. 1.2.30 (O. Langella, available from http://bioinformatics.org/~tryphon/populations/) with 500 bootstrap replications (on loci); and (b) corrected allele frequencies from FREENA (Chapuis & Estoup 2007) using TREEFIT (Kalinowski 2009). For (a), bootstrap values >50% are shown.</p>
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<caption>Supporting info item</caption>
</supportingInfoItem>
</supportingInformation>
<abstractGroup>
<abstract type="main" xml:lang="en">
<title type="main">Abstract</title>
<p>Most species with lengthy migrations display some degree of natal homing; some (e.g. migratory birds and anadromous salmonids) show spectacular feats of homing. However, studies of the sea lamprey (
<i>Petromyzon marinus</i>
) indicate that this anadromous species locates spawning habitat based on pheromonal cues from larvae rather than through philopatry. Previous genetic studies in the anadromous Pacific lamprey (
<i>Entosphenus tridentatus</i>
) have both supported and rejected the hypothesis of natal homing. To resolve this, we used nine microsatellite loci to examine the population structure in 965 Pacific lamprey from 20 locations from central British Columbia to southern California and supplemented this analysis with mitochondrial DNA restriction fragment length polymorphism analysis on a subset of 530 lamprey. Microsatellite analysis revealed (i) relatively low but often statistically significant genetic differentiation among locations (97% pairwise
<i>F</i>
<sub>ST</sub>
values were <0.04 but 73.7% were significant); and (ii) weak but significant isolation by distance (
<i>r</i>
<sup>2</sup>
 = 0.0565,
<i>P </i>
=
<i></i>
0.0450) but no geographic clustering of samples. The few moderate
<i>F</i>
<sub>ST</sub>
values involved comparisons with sites that were geographically distant or far upstream. The mtDNA analysis—although providing less resolution among sites (only 4.7%
<i>F</i>
<sub>ST</sub>
values were significant)—was broadly consistent with the microsatellite results: (i) the southernmost site and some sites tributary to the Salish Sea were genetically distinct; and (ii) southern sites showed higher haplotype and private haplotype richness. These results are inconsistent with philopatry, suggesting that anadromous lampreys are unusual among species with long migrations, but suggest that limited dispersal at sea precludes panmixia in this species.</p>
</abstract>
</abstractGroup>
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<titleInfo lang="en">
<title>Neither philopatric nor panmictic: microsatellite and mtDNA evidence suggests lack of natal homing but limits to dispersal in Pacific lamprey</title>
</titleInfo>
<titleInfo type="abbreviated" lang="en">
<title>ALTERNATE ANADROMY IN PACIFIC LAMPREY</title>
</titleInfo>
<titleInfo type="alternative" contentType="CDATA" lang="en">
<title>Neither philopatric nor panmictic: microsatellite and mtDNA evidence suggests lack of natal homing but limits to dispersal in Pacific lamprey</title>
</titleInfo>
<name type="personal">
<namePart type="given">ERIN K.</namePart>
<namePart type="family">SPICE</namePart>
<affiliation>Department of Biological Sciences, University of Manitoba, Winnipeg, Manitoba R3T 2N2, Canada</affiliation>
<role>
<roleTerm type="text">author</roleTerm>
</role>
</name>
<name type="personal">
<namePart type="given">DAMON H.</namePart>
<namePart type="family">GOODMAN</namePart>
<affiliation>U.S. Fish and Wildlife Service, 1655 Heindon Road, Arcata, CA 95521, USA</affiliation>
<role>
<roleTerm type="text">author</roleTerm>
</role>
</name>
<name type="personal">
<namePart type="given">STEWART B.</namePart>
<namePart type="family">REID</namePart>
<affiliation>Western Fishes, 2045 East Main Street, Ashland, OR 97520, USA</affiliation>
<role>
<roleTerm type="text">author</roleTerm>
</role>
</name>
<name type="personal">
<namePart type="given">MARGARET F.</namePart>
<namePart type="family">DOCKER</namePart>
<affiliation>Department of Biological Sciences, University of Manitoba, Winnipeg, Manitoba R3T 2N2, Canada</affiliation>
<role>
<roleTerm type="text">author</roleTerm>
</role>
</name>
<typeOfResource>text</typeOfResource>
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<publisher>Blackwell Publishing Ltd</publisher>
<place>
<placeTerm type="text">Oxford, UK</placeTerm>
</place>
<dateIssued encoding="w3cdtf">2012-06</dateIssued>
<edition>Received 26 October 2011; revision received 7 March 2012; accepted 13 March 2012</edition>
<copyrightDate encoding="w3cdtf">2012</copyrightDate>
</originInfo>
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<languageTerm type="code" authority="rfc3066">en</languageTerm>
<languageTerm type="code" authority="iso639-2b">eng</languageTerm>
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<abstract lang="en">Most species with lengthy migrations display some degree of natal homing; some (e.g. migratory birds and anadromous salmonids) show spectacular feats of homing. However, studies of the sea lamprey (Petromyzon marinus) indicate that this anadromous species locates spawning habitat based on pheromonal cues from larvae rather than through philopatry. Previous genetic studies in the anadromous Pacific lamprey (Entosphenus tridentatus) have both supported and rejected the hypothesis of natal homing. To resolve this, we used nine microsatellite loci to examine the population structure in 965 Pacific lamprey from 20 locations from central British Columbia to southern California and supplemented this analysis with mitochondrial DNA restriction fragment length polymorphism analysis on a subset of 530 lamprey. Microsatellite analysis revealed (i) relatively low but often statistically significant genetic differentiation among locations (97% pairwise FST values were <0.04 but 73.7% were significant); and (ii) weak but significant isolation by distance (r2 = 0.0565, P = 0.0450) but no geographic clustering of samples. The few moderate FST values involved comparisons with sites that were geographically distant or far upstream. The mtDNA analysis—although providing less resolution among sites (only 4.7%FST values were significant)—was broadly consistent with the microsatellite results: (i) the southernmost site and some sites tributary to the Salish Sea were genetically distinct; and (ii) southern sites showed higher haplotype and private haplotype richness. These results are inconsistent with philopatry, suggesting that anadromous lampreys are unusual among species with long migrations, but suggest that limited dispersal at sea precludes panmixia in this species.</abstract>
<subject lang="en">
<genre>keywords</genre>
<topic>anadromy</topic>
<topic>Entosphenus</topic>
<topic>microsatellite</topic>
<topic>Pacific lamprey</topic>
<topic>philopatry</topic>
<topic>population structure</topic>
</subject>
<relatedItem type="host">
<titleInfo>
<title>Molecular Ecology</title>
</titleInfo>
<genre type="journal">journal</genre>
<note type="content"> Table S1 Summary statistics for each locus in Pacific lamprey (Entosphenus tridentatus) collected at 20 sites along the west coast of North America.Table S2 Comparison of pairwise FST values generated from original (above the diagonal) and null allele corrected (below the diagonal) data, for Pacific lamprey (Entosphenus tridentatus) collected at 20 sites along the west coast of North America.Table S3 Global FST (g FST) per locus estimated with and without the ENA correction described in Chapuis & Estoup (2007).Table S4 Comparison of pairwise FST values calculated using GENEPOP v. 4.0.10 (Raymond & Rousset 1995; Rousset 2008) both with (above diagonal) and without (below diagonal) loci Etr‐2, Etr‐3, and Lri‐3 for Pacific lamprey (Entosphenus tridentatus) collected at 20 sites along the west coast of North America.Table S5 Results of Colony (Jones & Wang 2010) sibship analysis for Pacific lamprey (Entosphenus tridentatus) collected at 20 sites along the west coast of North America.Table S6 Jost’s D values calculated using SMOGD v.1.2.5 (Crawford 2010) for Pacific lamprey (Entosphenus tridentatus) collected at 20 sites along the west coast of North America.Table S7 Restriction fragment length polymorphism (RFLP) composite haplotype frequencies for Pacific lamprey (Entosphenus tridentatus) collected at 20 sites along the west coast of North America, following Goodman et al. (2008); haplotype richness and private haplotype richness were calculated using rarefaction implemented in HP‐Rare (Kalinowski 2005).Fig. S1 Neighbor‐joining trees produced with: (a) original data set using POPULATIONS v. 1.2.30 (O. Langella, available from http://bioinformatics.org/~tryphon/populations/) with 500 bootstrap replications (on loci); and (b) corrected allele frequencies from FREENA (Chapuis & Estoup 2007) using TREEFIT (Kalinowski 2009). For (a), bootstrap values >50% are shown.Supporting Info Item: Supporting info item - </note>
<identifier type="ISSN">0962-1083</identifier>
<identifier type="eISSN">1365-294X</identifier>
<identifier type="DOI">10.1111/(ISSN)1365-294X</identifier>
<identifier type="PublisherID">MEC</identifier>
<part>
<date>2012</date>
<detail type="volume">
<caption>vol.</caption>
<number>21</number>
</detail>
<detail type="issue">
<caption>no.</caption>
<number>12</number>
</detail>
<extent unit="pages">
<start>2916</start>
<end>2930</end>
<total>15</total>
</extent>
</part>
</relatedItem>
<identifier type="istex">48918E62DF873F53D92128F443136EBCB4A3168D</identifier>
<identifier type="DOI">10.1111/j.1365-294X.2012.05585.x</identifier>
<identifier type="ArticleID">MEC5585</identifier>
<accessCondition type="use and reproduction" contentType="copyright">© 2012 Blackwell Publishing Ltd</accessCondition>
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