To remain or leave: Dispersal variation and its genetic consequences in benthic freshwater invertebrates
Abstract Variation in dispersal capacity may influence population genetic variation and relatedness of freshwater animals thus demonstrating how life‐history traits influence patterns and processes that in turn influence biodiversity. The majority of studies have focused on the consequences of dispe...
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doaj-6cad7a8c934240ba81f9820fab9ab5db2021-04-02T13:08:26ZengWileyEcology and Evolution2045-77582019-11-01921120691208810.1002/ece3.5656To remain or leave: Dispersal variation and its genetic consequences in benthic freshwater invertebratesPaolo Ruggeri0Ellen Pasternak1Beth Okamura2Department of Life Sciences Natural History Museum London UKDepartment of Life Sciences Natural History Museum London UKDepartment of Life Sciences Natural History Museum London UKAbstract Variation in dispersal capacity may influence population genetic variation and relatedness of freshwater animals thus demonstrating how life‐history traits influence patterns and processes that in turn influence biodiversity. The majority of studies have focused on the consequences of dispersal variation in taxa inhabiting riverine systems whose dendritic nature and upstream/downstream gradients facilitate characterizing populations along networks. We undertook extensive, large‐scale investigations of the impacts of hydrological connectivity on population genetic variation in two freshwater bryozoan species whose dispersive propagules (statoblasts) are either attached to surfaces (Fredericella sultana) or are released as buoyant stages (Cristatella mucedo) and that live primarily in either lotic (F. sultana) or lentic environments (C. mucedo). Describing population genetic structure in multiple sites characterized by varying degrees of hydrological connectivity within each of three (or four) UK regions enabled us to test the following hypotheses: (1) genetic diversity and gene flow will be more influenced by hydrological connectivity in populations of C. mucedo (because F. sultana dispersal stages are retained); (2) populations of F. sultana will be characterized by greater genetic divergence than those of C. mucedo (reflecting their relative dispersal capacities); and (3) genetic variation will be greatest in F. sultana (reflecting a propensity for genetic divergence as a result of its low dispersal potential). We found that hydrological connectivity enhanced genetic diversity and gene flow among C. mucedo populations but not in F. sultana while higher overall measures of clonal diversity and greater genetic divergence characterized populations of F. sultana. We suggest that genetic divergence over time within F. sultana populations reflects a general constraint of releasing propagules that might eventually be swept to sea when taxa inhabit running waters. In contrast, taxa that primarily inhabit lakes and ponds may colonize across hydrologically connected regions, establishing genetically related populations. Our study contributes more nuanced views about drivers of population genetic structures in passively dispersing freshwater invertebrates as outlined by the Monopolization Hypothesis (Acta Oecologica, 23, 2002, 121) by highlighting how a range of demographic and evolutionary processes reflect life‐history attributes of benthic colonial invertebrates (bryozoans) and cyclically parthenogenetic zooplankton. In addition, growing evidence that genetic divergence may commonly characterize populations of diverse groups of riverine taxa suggests that organisms inhabiting lotic systems may be particularly challenged by environmental change. Such change may predispose riverine populations to extinction as a result of genetic divergence combined with limited dispersal and gene flow. Open Research Badges This article has earned an Open Data Badge for making publicly available the digitally‐shareable data necessary to reproduce the reported results. The data is available at https://doi.org/10.5061/dryad.1tm8705.https://doi.org/10.1002/ece3.5656Cristatella mucedodispersal abilityFredericella sultanagene flowhydrological connectivitystatoblasts |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Paolo Ruggeri Ellen Pasternak Beth Okamura |
spellingShingle |
Paolo Ruggeri Ellen Pasternak Beth Okamura To remain or leave: Dispersal variation and its genetic consequences in benthic freshwater invertebrates Ecology and Evolution Cristatella mucedo dispersal ability Fredericella sultana gene flow hydrological connectivity statoblasts |
author_facet |
Paolo Ruggeri Ellen Pasternak Beth Okamura |
author_sort |
Paolo Ruggeri |
title |
To remain or leave: Dispersal variation and its genetic consequences in benthic freshwater invertebrates |
title_short |
To remain or leave: Dispersal variation and its genetic consequences in benthic freshwater invertebrates |
title_full |
To remain or leave: Dispersal variation and its genetic consequences in benthic freshwater invertebrates |
title_fullStr |
To remain or leave: Dispersal variation and its genetic consequences in benthic freshwater invertebrates |
title_full_unstemmed |
To remain or leave: Dispersal variation and its genetic consequences in benthic freshwater invertebrates |
title_sort |
to remain or leave: dispersal variation and its genetic consequences in benthic freshwater invertebrates |
publisher |
Wiley |
series |
Ecology and Evolution |
issn |
2045-7758 |
publishDate |
2019-11-01 |
description |
Abstract Variation in dispersal capacity may influence population genetic variation and relatedness of freshwater animals thus demonstrating how life‐history traits influence patterns and processes that in turn influence biodiversity. The majority of studies have focused on the consequences of dispersal variation in taxa inhabiting riverine systems whose dendritic nature and upstream/downstream gradients facilitate characterizing populations along networks. We undertook extensive, large‐scale investigations of the impacts of hydrological connectivity on population genetic variation in two freshwater bryozoan species whose dispersive propagules (statoblasts) are either attached to surfaces (Fredericella sultana) or are released as buoyant stages (Cristatella mucedo) and that live primarily in either lotic (F. sultana) or lentic environments (C. mucedo). Describing population genetic structure in multiple sites characterized by varying degrees of hydrological connectivity within each of three (or four) UK regions enabled us to test the following hypotheses: (1) genetic diversity and gene flow will be more influenced by hydrological connectivity in populations of C. mucedo (because F. sultana dispersal stages are retained); (2) populations of F. sultana will be characterized by greater genetic divergence than those of C. mucedo (reflecting their relative dispersal capacities); and (3) genetic variation will be greatest in F. sultana (reflecting a propensity for genetic divergence as a result of its low dispersal potential). We found that hydrological connectivity enhanced genetic diversity and gene flow among C. mucedo populations but not in F. sultana while higher overall measures of clonal diversity and greater genetic divergence characterized populations of F. sultana. We suggest that genetic divergence over time within F. sultana populations reflects a general constraint of releasing propagules that might eventually be swept to sea when taxa inhabit running waters. In contrast, taxa that primarily inhabit lakes and ponds may colonize across hydrologically connected regions, establishing genetically related populations. Our study contributes more nuanced views about drivers of population genetic structures in passively dispersing freshwater invertebrates as outlined by the Monopolization Hypothesis (Acta Oecologica, 23, 2002, 121) by highlighting how a range of demographic and evolutionary processes reflect life‐history attributes of benthic colonial invertebrates (bryozoans) and cyclically parthenogenetic zooplankton. In addition, growing evidence that genetic divergence may commonly characterize populations of diverse groups of riverine taxa suggests that organisms inhabiting lotic systems may be particularly challenged by environmental change. Such change may predispose riverine populations to extinction as a result of genetic divergence combined with limited dispersal and gene flow. Open Research Badges This article has earned an Open Data Badge for making publicly available the digitally‐shareable data necessary to reproduce the reported results. The data is available at https://doi.org/10.5061/dryad.1tm8705. |
topic |
Cristatella mucedo dispersal ability Fredericella sultana gene flow hydrological connectivity statoblasts |
url |
https://doi.org/10.1002/ece3.5656 |
work_keys_str_mv |
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