Differential dispersal shapes population structure and patterns of genetic differentiation in two sympatric pond breeding salamanders

Peterman, William E.; Anderson, Thomas L.; Ousterhout, Brittany H.; Drake, Dana L.; Semlitsch, Raymond D.; Eggert, Lori S.

doi:10.1007/s10592-014-0640-x

Cited by 39 publications

(57 citation statements)

References 57 publications

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“…Due to their low dispersal abilities (Bowne & Bowers, ; Graeter, Rothermel, & Gibbons, ), small effective population sizes (Funk, Tallmon, & Allendorf, ) and the discontinuous distribution of their preferred breeding habitats (Jehle, Burke, & Arntzen, ), they tend to form “patchy” breeding assemblages. Dispersal and the maintenance of gene flow between breeding ponds depends on the composition and configuration of the landscape (Coster et al., ), and studies focusing on functional connectivity have described different species responses to landscape features such as differences in soil moisture, clear‐cut habitats, agriculture lands, riparian network, as well as differences in metamorphosis, philopatry, dispersal, selection of breeding sites and post‐breeding behaviour (Coster et al., ; Goldberg & Waits, ; Peterman et al., ; Richardson, ; Steele et al., ). Identification of the factors promoting or reducing gene flow is key to prevent local and regional extinctions in the long‐term and to inform conservation management.…”

Section: Introductionmentioning

confidence: 99%

Comparative landscape genetics of pond‐breeding amphibians in Mediterranean temporal wetlands: The positive role of structural heterogeneity in promoting gene flow

et al. 2017

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Comparative landscape genetics studies can provide key information to implement cost-effective conservation measures favouring a broad set of taxa. These studies are scarce, particularly in Mediterranean areas, which include diverse but threatened biological communities. Here, we focus on Mediterranean wetlands in central Iberia and perform a multi-level, comparative study of two endemic pond-breeding amphibians, a salamander (Pleurodeles waltl) and a toad (Pelobates cultripes). We genotyped 411 salamanders from 20 populations and 306 toads from 16 populations at 18 and 16 microsatellite loci, respectively, and identified major factors associated with population connectivity through the analysis of three sets of variables potentially affecting gene flow at increasingly finer levels of spatial resolution. Topographic, land use/cover, and remotely sensed vegetation/moisture indices were used to derive optimized resistance surfaces for the two species. We found contrasting patterns of genetic structure, with stronger, finer scale genetic differentiation in Pleurodeles waltl, and notable differences in the role of fine-scale patterns of heterogeneity in vegetation cover and water content in shaping patterns of regional genetic structure in the two species. Overall, our results suggest a positive role of structural heterogeneity in population connectivity in pond-breeding amphibians, with habitat patches of Mediterranean scrubland and open oak woodlands ("dehesas") facilitating gene flow. Our study highlights the usefulness of remotely sensed continuous variables of land cover, vegetation and water content (e.g., NDVI, NDMI) in conservation-oriented studies aimed at identifying major drivers of population connectivity.

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Section: Introductionmentioning

confidence: 99%

Comparative landscape genetics of pond‐breeding amphibians in Mediterranean temporal wetlands: The positive role of structural heterogeneity in promoting gene flow

et al. 2017

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“…These regions are dominated by temperate broadleaf and mixed forests (Ouachita Ecoregional Assessment Team, 2003;Ozarks Ecoregional Assessment Team, 2003). salamanders shows that effective population size and genetic diversity does not significantly differ among life stages (Peterman, Brocato, Semlitsch, & Eggert, 2016) and genetic inference is largely concordant among breeding seasons across the same landscape (Burkhart et al, 2017;Peterman et al, 2015). In total, we in Ambystoma spp.…”

Section: Study Area and Sample Collectionmentioning

confidence: 86%

“…More recent studies using microsatellite loci observed two genetic clusters over an approximately 7,000 ha landscape (Burkhart et al, 2017;Peterman et al, 2015), which indicates the potential for dispersal limitation over more ecological time frames.…”

Section: Introductionmentioning

confidence: 92%

Post‐Pleistocene differentiation in a Central Interior Highlands endemic salamander

Burkhart

Puckett

Beringer

et al. 2019

Ecology and Evolution

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Aim For many endemic species with limited dispersal capacities, the relationship between landscape changes and species distributions is still unclear. We characterized the population structure of the endemic ringed salamander (Ambystoma annulatum) across its distribution in the Central Interior Highlands (CIH) of North America, an area of high species endemism, to infer the ecological and evolutionary history of the species. Methods We sampled 498 individuals across the species distribution and characterized the population genetic structure using nuclear microsatellite and mitochondrial DNA (mtDNA) markers. Results Ambystoma annulatum exist in two strongly supported nuclear genetic clusters across the CIH that correspond to a northern cluster that includes the Missouri Ozark populations and a southern cluster that includes the Arkansas and Oklahoma Ozarks and the Ouachita Mountains. Our demographic models estimated that these populations diverged approximately 2,700 years ago. Pairwise estimates of genetic differentiation at microsatellite and mtDNA markers indicated limited contemporary gene flow and suggest that genetic differentiation was primarily influenced by changes in the post‐Pleistocene landscape of the CIH. Main Conclusions Both the geologic history and post‐European settlement history of the CIH have influenced the population genetic structure of A. annulatum. The low mtDNA diversity suggests a retraction into and expansion out of refugial areas in the south‐central Ozarks, during temperature fluctuations of the Pleistocene and Holocene epochs. Similarly, the estimated divergence time for the two nuclear clusters corresponds to changes in the post‐Pleistocene landscape. More recently, decreased A. annulatum gene flow may be a result of increased habitat fragmentation and alteration post‐European settlement.

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“…We therefore relied on Gamble et al () to guide our estimate of a plausible distribution for this parameter, setting the mean to 0.85 ± 0.10 (truncating the upper limit at 1.0). Because previous research in this system reported minimal influence of the landscape matrix on genetic connectivity of ringed salamanders (Peterman et al , ; Burkhart et al ), we modeled dispersal and connectivity as an exponential decay of distance. We drew mean dispersal distance from a normal distribution with a mean of 1,700 m (±500 m SD) derived from genetic‐based dispersal estimates for ringed salamanders at FLW (Peterman et al ).…”

Section: Methodsmentioning

confidence: 99%

“…Because previous research in this system reported minimal influence of the landscape matrix on genetic connectivity of ringed salamanders (Peterman et al , ; Burkhart et al ), we modeled dispersal and connectivity as an exponential decay of distance. We drew mean dispersal distance from a normal distribution with a mean of 1,700 m (±500 m SD) derived from genetic‐based dispersal estimates for ringed salamanders at FLW (Peterman et al ). We calculated the probability of successful dispersal from population i to population j as

m_{i j} = true{\begin{matrix} center \\ center \exp true(- {normalα normald}_{normali normalj} true) i f i \neq j \\ center 0 i f i = j \end{matrix}

where d ij is the distance between populations and α controls the dispersal range, with 1 /α being the average dispersal distance.…”

Section: Methodsmentioning

confidence: 99%

Using spatial demographic network models to optimize habitat management decisions

et al. 2017

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Conservation and management activities are always constrained by finite resources. Therefore, decisions such as which sites to protect, whether existing habitat should be restored or whether new habitat should be created, and where on the landscape management efforts should be focused present difficult challenges. An overarching goal of many conservation or management plans is the long‐term persistence of populations, which is often dependent on functional connectivity and the maintenance of metapopulation dynamics. Graph theory and network approaches are frequently used tools for modeling functional connections between populations and between habitats. Less often, graph models are used to guide conservation or management decisions. We used spatial networks derived for an amphibian population to determine optimal locations to create new habitat, prioritize existing habitat for restoration, and determine the habitat most critical for maintaining connectivity within the existing metapopulation within Fort Leonard Wood, Missouri, USA, 2012–2014. Using data collected at 206 breeding ponds over 3 years, we constructed demographic networks representing the functional connectivity between ponds by dispersing ringed salamanders (Ambystoma annulatum). We incorporated uncertainty in key model parameters through Monte Carlo simulation, and used a graph‐theoretical parameterization of the metapopulation mean lifetime model to assess how changes in network structure affect persistence of the network. We conducted addition and removal experiments within our Monte Carlo simulations to rank and prioritize locations for pond creation, ponds for restoration, and ponds for preservation. Salamanders bred in 106 ponds in ≥1 year; 2.4% of ponds functioned predominantly as sources and 51% of occupied ponds functioned predominantly as sinks. The importance of a pond to the network was correlated with the number of emigrants dispersing from a pond, the number of ponds reached by these dispersers, and the frequency a pond functioned as a source. Creating new ponds at optimal locations increased the persistence of the network an average of 15.4% compared to randomly selected locations, whereas selective restoration of currently unoccupied ponds resulted in an average increase of 31.4% in network persistence, as compared to randomly selected unoccupied ponds. Through Monte Carlo simulation, we constructed biologically informed demographic connectivity networks for use as a spatial conservation or management planning tool. Although our approach was implemented with an amphibian and a breeding pond network, it is generalizable to any species occupying discrete habitat patches. © 2017 The Wildlife Society.

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Differential dispersal shapes population structure and patterns of genetic differentiation in two sympatric pond breeding salamanders

Cited by 39 publications

References 57 publications

Comparative landscape genetics of pond‐breeding amphibians in Mediterranean temporal wetlands: The positive role of structural heterogeneity in promoting gene flow

Comparative landscape genetics of pond‐breeding amphibians in Mediterranean temporal wetlands: The positive role of structural heterogeneity in promoting gene flow

Post‐Pleistocene differentiation in a Central Interior Highlands endemic salamander

Using spatial demographic network models to optimize habitat management decisions

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