Is variable connectivity among populations of a continental gobiid fish driven by local adaptation or passive dispersal?

Joel Huey, David Crook, Jed Macdonald, Daniel Schmidt, Jonathan Marshall, Stephen Balcombe, Ryan Woods, Jane Hughes

    Research output: Contribution to journalArticleResearchpeer-review

    Abstract

    1.   Amphidromy, thedispersal of larvae to the estuarine or marine environment with juvenilesrecolonising fresh waters to complete development, is common on tropicalislands. This has led to the suggestion that amphidromy is an adaptation tohydrologically unpredictable environments, allowing recolonisation after localextinction (dispersal-limitation hypothesis). Alternatively, amphidromy may bemore common in streams with stronger flow, as high tractive forces flush larvaeinto the estuarine/marine environment, forcing them to recolonise (passivedispersal hypothesis).

     

    2.   We tested thesehypotheses in a continental gobiid fish, the Roman Nose Goby (Awaous acritosus)that inhabits hydrologically and physically diverse catchments on the eastcoast of Australia. We measured 87Sr/86Sr along transects of the otoliths of 92adult fish from 12 catchments, identified migratory life histories from thesedata and correlated the proportion of migratory fish with key environmentalvariables. This information was augmented with data from mtDNA (n = 276) andsix microsatellite loci (n = 429) from 19 catchments, to explore gene flowamong catchments and to assess whether local adaptation was likely in the faceof high or restricted gene flow.

     

    3.   Estimates of87Sr/86Sr along transects revealed high variation in life history, with 63% ofindividuals showing no evidence of marine/estuarine residence. The slope ofcatchments was the only significant variable associated with the proportion oflarvae retained in catchments, with steep catchments having a greaterproportion of adults exhibiting a marine/estuarine phase during early life.Total panmixia was detected with mtDNA and six microsatellite loci, suggestingthat gene flow is high for this species.

     

    4.   These results supportthe passive dispersal hypothesis. Steep slopes are likely to have higher tractiveforces in their flow, leading to a greater proportion of larvae being flushedinto the estuary or sea. In addition, high gene flow would inhibit localadaptation, making the dispersal-limitation hypothesis unlikely.

     

    5.      This study provides aframework for understanding how local adaptation may be constrained by geneflow across the landscape so that the adaptive or passive mechanism underlyingfacultative amphidromy can be explored.

    Original languageEnglish
    Pages (from-to)1672-1686
    Number of pages15
    JournalFreshwater Biology
    Volume59
    Issue number8
    DOIs
    Publication statusPublished - Aug 2014

    Fingerprint

    local adaptation
    connectivity
    catchment
    fish
    estuarine environment
    marine environment
    gene flow
    life history
    mitochondrial DNA
    transect
    microsatellite repeats
    larva
    loci
    gene
    larvae
    recolonization
    otolith
    otoliths
    genes
    estuaries

    Cite this

    Huey, Joel ; Crook, David ; Macdonald, Jed ; Schmidt, Daniel ; Marshall, Jonathan ; Balcombe, Stephen ; Woods, Ryan ; Hughes, Jane. / Is variable connectivity among populations of a continental gobiid fish driven by local adaptation or passive dispersal?. In: Freshwater Biology. 2014 ; Vol. 59, No. 8. pp. 1672-1686.
    @article{7d4bd07311e347d2929e676e81bdeb05,
    title = "Is variable connectivity among populations of a continental gobiid fish driven by local adaptation or passive dispersal?",
    abstract = "1.   Amphidromy, thedispersal of larvae to the estuarine or marine environment with juvenilesrecolonising fresh waters to complete development, is common on tropicalislands. This has led to the suggestion that amphidromy is an adaptation tohydrologically unpredictable environments, allowing recolonisation after localextinction (dispersal-limitation hypothesis). Alternatively, amphidromy may bemore common in streams with stronger flow, as high tractive forces flush larvaeinto the estuarine/marine environment, forcing them to recolonise (passivedispersal hypothesis). 2.   We tested thesehypotheses in a continental gobiid fish, the Roman Nose Goby (Awaous acritosus)that inhabits hydrologically and physically diverse catchments on the eastcoast of Australia. We measured 87Sr/86Sr along transects of the otoliths of 92adult fish from 12 catchments, identified migratory life histories from thesedata and correlated the proportion of migratory fish with key environmentalvariables. This information was augmented with data from mtDNA (n = 276) andsix microsatellite loci (n = 429) from 19 catchments, to explore gene flowamong catchments and to assess whether local adaptation was likely in the faceof high or restricted gene flow. 3.   Estimates of87Sr/86Sr along transects revealed high variation in life history, with 63{\%} ofindividuals showing no evidence of marine/estuarine residence. The slope ofcatchments was the only significant variable associated with the proportion oflarvae retained in catchments, with steep catchments having a greaterproportion of adults exhibiting a marine/estuarine phase during early life.Total panmixia was detected with mtDNA and six microsatellite loci, suggestingthat gene flow is high for this species. 4.   These results supportthe passive dispersal hypothesis. Steep slopes are likely to have higher tractiveforces in their flow, leading to a greater proportion of larvae being flushedinto the estuary or sea. In addition, high gene flow would inhibit localadaptation, making the dispersal-limitation hypothesis unlikely. 5.      This study provides aframework for understanding how local adaptation may be constrained by geneflow across the landscape so that the adaptive or passive mechanism underlyingfacultative amphidromy can be explored.",
    keywords = "Awaous, Callogobius atratus, Gobiidae",
    author = "Joel Huey and David Crook and Jed Macdonald and Daniel Schmidt and Jonathan Marshall and Stephen Balcombe and Ryan Woods and Jane Hughes",
    year = "2014",
    month = "8",
    doi = "10.1111/fwb.12373",
    language = "English",
    volume = "59",
    pages = "1672--1686",
    journal = "Freshwater Biology",
    issn = "0046-5070",
    publisher = "Blackwell Publishing Ltd",
    number = "8",

    }

    Huey, J, Crook, D, Macdonald, J, Schmidt, D, Marshall, J, Balcombe, S, Woods, R & Hughes, J 2014, 'Is variable connectivity among populations of a continental gobiid fish driven by local adaptation or passive dispersal?', Freshwater Biology, vol. 59, no. 8, pp. 1672-1686. https://doi.org/10.1111/fwb.12373

    Is variable connectivity among populations of a continental gobiid fish driven by local adaptation or passive dispersal? / Huey, Joel; Crook, David; Macdonald, Jed; Schmidt, Daniel; Marshall, Jonathan; Balcombe, Stephen; Woods, Ryan; Hughes, Jane.

    In: Freshwater Biology, Vol. 59, No. 8, 08.2014, p. 1672-1686.

    Research output: Contribution to journalArticleResearchpeer-review

    TY - JOUR

    T1 - Is variable connectivity among populations of a continental gobiid fish driven by local adaptation or passive dispersal?

    AU - Huey, Joel

    AU - Crook, David

    AU - Macdonald, Jed

    AU - Schmidt, Daniel

    AU - Marshall, Jonathan

    AU - Balcombe, Stephen

    AU - Woods, Ryan

    AU - Hughes, Jane

    PY - 2014/8

    Y1 - 2014/8

    N2 - 1.   Amphidromy, thedispersal of larvae to the estuarine or marine environment with juvenilesrecolonising fresh waters to complete development, is common on tropicalislands. This has led to the suggestion that amphidromy is an adaptation tohydrologically unpredictable environments, allowing recolonisation after localextinction (dispersal-limitation hypothesis). Alternatively, amphidromy may bemore common in streams with stronger flow, as high tractive forces flush larvaeinto the estuarine/marine environment, forcing them to recolonise (passivedispersal hypothesis). 2.   We tested thesehypotheses in a continental gobiid fish, the Roman Nose Goby (Awaous acritosus)that inhabits hydrologically and physically diverse catchments on the eastcoast of Australia. We measured 87Sr/86Sr along transects of the otoliths of 92adult fish from 12 catchments, identified migratory life histories from thesedata and correlated the proportion of migratory fish with key environmentalvariables. This information was augmented with data from mtDNA (n = 276) andsix microsatellite loci (n = 429) from 19 catchments, to explore gene flowamong catchments and to assess whether local adaptation was likely in the faceof high or restricted gene flow. 3.   Estimates of87Sr/86Sr along transects revealed high variation in life history, with 63% ofindividuals showing no evidence of marine/estuarine residence. The slope ofcatchments was the only significant variable associated with the proportion oflarvae retained in catchments, with steep catchments having a greaterproportion of adults exhibiting a marine/estuarine phase during early life.Total panmixia was detected with mtDNA and six microsatellite loci, suggestingthat gene flow is high for this species. 4.   These results supportthe passive dispersal hypothesis. Steep slopes are likely to have higher tractiveforces in their flow, leading to a greater proportion of larvae being flushedinto the estuary or sea. In addition, high gene flow would inhibit localadaptation, making the dispersal-limitation hypothesis unlikely. 5.      This study provides aframework for understanding how local adaptation may be constrained by geneflow across the landscape so that the adaptive or passive mechanism underlyingfacultative amphidromy can be explored.

    AB - 1.   Amphidromy, thedispersal of larvae to the estuarine or marine environment with juvenilesrecolonising fresh waters to complete development, is common on tropicalislands. This has led to the suggestion that amphidromy is an adaptation tohydrologically unpredictable environments, allowing recolonisation after localextinction (dispersal-limitation hypothesis). Alternatively, amphidromy may bemore common in streams with stronger flow, as high tractive forces flush larvaeinto the estuarine/marine environment, forcing them to recolonise (passivedispersal hypothesis). 2.   We tested thesehypotheses in a continental gobiid fish, the Roman Nose Goby (Awaous acritosus)that inhabits hydrologically and physically diverse catchments on the eastcoast of Australia. We measured 87Sr/86Sr along transects of the otoliths of 92adult fish from 12 catchments, identified migratory life histories from thesedata and correlated the proportion of migratory fish with key environmentalvariables. This information was augmented with data from mtDNA (n = 276) andsix microsatellite loci (n = 429) from 19 catchments, to explore gene flowamong catchments and to assess whether local adaptation was likely in the faceof high or restricted gene flow. 3.   Estimates of87Sr/86Sr along transects revealed high variation in life history, with 63% ofindividuals showing no evidence of marine/estuarine residence. The slope ofcatchments was the only significant variable associated with the proportion oflarvae retained in catchments, with steep catchments having a greaterproportion of adults exhibiting a marine/estuarine phase during early life.Total panmixia was detected with mtDNA and six microsatellite loci, suggestingthat gene flow is high for this species. 4.   These results supportthe passive dispersal hypothesis. Steep slopes are likely to have higher tractiveforces in their flow, leading to a greater proportion of larvae being flushedinto the estuary or sea. In addition, high gene flow would inhibit localadaptation, making the dispersal-limitation hypothesis unlikely. 5.      This study provides aframework for understanding how local adaptation may be constrained by geneflow across the landscape so that the adaptive or passive mechanism underlyingfacultative amphidromy can be explored.

    KW - Awaous

    KW - Callogobius atratus

    KW - Gobiidae

    UR - http://www.scopus.com/inward/record.url?scp=84903769115&partnerID=8YFLogxK

    U2 - 10.1111/fwb.12373

    DO - 10.1111/fwb.12373

    M3 - Article

    VL - 59

    SP - 1672

    EP - 1686

    JO - Freshwater Biology

    JF - Freshwater Biology

    SN - 0046-5070

    IS - 8

    ER -