Evolutionary dynamics inform management interventions of a hanging garden obligate, Carex specuicola

Uncovering the historical and contemporary processes shaping rare species with complex distributions is of growing importance due to threats such as habitat destruction and climate change. Species restricted to specialized, patchy habitat may persist by virtue of life history characteristics facilit...

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Main Authors: Kenneth James Chapin, Matthew R. Jones, Daniel E. Winkler, Glenn Rink, Rob Massatti
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-10-01
Series:Frontiers in Conservation Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fcosc.2022.941002/full
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author Kenneth James Chapin
Matthew R. Jones
Daniel E. Winkler
Glenn Rink
Rob Massatti
author_facet Kenneth James Chapin
Matthew R. Jones
Daniel E. Winkler
Glenn Rink
Rob Massatti
author_sort Kenneth James Chapin
collection DOAJ
description Uncovering the historical and contemporary processes shaping rare species with complex distributions is of growing importance due to threats such as habitat destruction and climate change. Species restricted to specialized, patchy habitat may persist by virtue of life history characteristics facilitating ongoing gene flow and dispersal, but they could also reflect the remnants of formerly widespread, suitable habitat that existed during past climate regimes. If formerly widespread species did not rely upon traits facilitating high dispersibility to persist, contemporary populations could be at high risk of extirpation or extinction. Fortunately, genomic investigations provide an opportunity to illuminate such alternative scenarios while simultaneously offering guidance for future management interventions. Herein, we test the role of these mechanisms in shaping patterns of genomic diversity and differentiation across a highly restricted and rare ecosystem: desert hanging gardens. We focus on Carex specuicola (Cyperaceae), a hanging garden obligate narrowly distributed in the Four Corners region of the southwestern United States that is listed as Threatened under the United States Endangered Species Act. Population structure and diversity analyses reveal that hanging garden populations are shaped by strong genetic drift, but that individuals in gardens are occasionally more closely related to individuals at other gardens than to individuals within the same garden. Similarly, gardens separated by long geographic distances may contain individuals that are more closely related compared to individuals in gardens separated by short geographic distances. Demographic modeling supports historical gene flow between some contemporary garden pairs, which is corroborated by low estimates of inbreeding coefficients and recent divergence times. As such, multiple lines of evidence support dispersal and gene flow across C. specuicola populations at both small and large spatial scales, indicating that even if C. specuicola was formerly more widespread, it may be well suited to persist in hanging gardens so long as suitable habitat remains available. Analyses like those demonstrated herein may be broadly applicable for understanding the short- and long-term evolutionary processes influencing rare species, and especially those having complex distributions across heterogeneous landscapes.
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spelling doaj.art-2a37db9b52a449208932a6532aa6ccd82022-12-22T03:53:15ZengFrontiers Media S.A.Frontiers in Conservation Science2673-611X2022-10-01310.3389/fcosc.2022.941002941002Evolutionary dynamics inform management interventions of a hanging garden obligate, Carex specuicolaKenneth James Chapin0Matthew R. Jones1Daniel E. Winkler2Glenn Rink3Rob Massatti4US Geological Survey, Southwest Biological Science Center, Tucson, AZ, United StatesUS Geological Survey, Southwest Biological Science Center, Flagstaff, AZ, United StatesUS Geological Survey, Southwest Biological Science Center, Tucson, AZ, United StatesDeaver Herbarium, Northern Arizona University, Flagstaff, AZ, United StatesUS Geological Survey, Southwest Biological Science Center, Flagstaff, AZ, United StatesUncovering the historical and contemporary processes shaping rare species with complex distributions is of growing importance due to threats such as habitat destruction and climate change. Species restricted to specialized, patchy habitat may persist by virtue of life history characteristics facilitating ongoing gene flow and dispersal, but they could also reflect the remnants of formerly widespread, suitable habitat that existed during past climate regimes. If formerly widespread species did not rely upon traits facilitating high dispersibility to persist, contemporary populations could be at high risk of extirpation or extinction. Fortunately, genomic investigations provide an opportunity to illuminate such alternative scenarios while simultaneously offering guidance for future management interventions. Herein, we test the role of these mechanisms in shaping patterns of genomic diversity and differentiation across a highly restricted and rare ecosystem: desert hanging gardens. We focus on Carex specuicola (Cyperaceae), a hanging garden obligate narrowly distributed in the Four Corners region of the southwestern United States that is listed as Threatened under the United States Endangered Species Act. Population structure and diversity analyses reveal that hanging garden populations are shaped by strong genetic drift, but that individuals in gardens are occasionally more closely related to individuals at other gardens than to individuals within the same garden. Similarly, gardens separated by long geographic distances may contain individuals that are more closely related compared to individuals in gardens separated by short geographic distances. Demographic modeling supports historical gene flow between some contemporary garden pairs, which is corroborated by low estimates of inbreeding coefficients and recent divergence times. As such, multiple lines of evidence support dispersal and gene flow across C. specuicola populations at both small and large spatial scales, indicating that even if C. specuicola was formerly more widespread, it may be well suited to persist in hanging gardens so long as suitable habitat remains available. Analyses like those demonstrated herein may be broadly applicable for understanding the short- and long-term evolutionary processes influencing rare species, and especially those having complex distributions across heterogeneous landscapes.https://www.frontiersin.org/articles/10.3389/fcosc.2022.941002/fulldemographic modelingmetapopulationpaleorefugiahanging gardenphylogeographypopulation genetics
spellingShingle Kenneth James Chapin
Matthew R. Jones
Daniel E. Winkler
Glenn Rink
Rob Massatti
Evolutionary dynamics inform management interventions of a hanging garden obligate, Carex specuicola
Frontiers in Conservation Science
demographic modeling
metapopulation
paleorefugia
hanging garden
phylogeography
population genetics
title Evolutionary dynamics inform management interventions of a hanging garden obligate, Carex specuicola
title_full Evolutionary dynamics inform management interventions of a hanging garden obligate, Carex specuicola
title_fullStr Evolutionary dynamics inform management interventions of a hanging garden obligate, Carex specuicola
title_full_unstemmed Evolutionary dynamics inform management interventions of a hanging garden obligate, Carex specuicola
title_short Evolutionary dynamics inform management interventions of a hanging garden obligate, Carex specuicola
title_sort evolutionary dynamics inform management interventions of a hanging garden obligate carex specuicola
topic demographic modeling
metapopulation
paleorefugia
hanging garden
phylogeography
population genetics
url https://www.frontiersin.org/articles/10.3389/fcosc.2022.941002/full
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