A Tale of Two Amphibians: Urban Landscapes Differentially Impact Gene Flow

When we think of urban organisms, we often don’t think of aquatic organisms. But wetlands exist in the urban matrix, and aquatic and amphibious species are impacted by habitat changes associated with urbanization. A recent study published in Ecology and Evolution by Jared Homola, Cynthia Loftin, and Michael Kinnison dug into the population genetics of two common pond-breeding amphibians in Maine: spotted salamanders (Ambystoma maculatum) and wood frogs (Lithobates sylvaticus). These two species form metapopulations, meaning they move between areas of high-quality habitat (wetlands) across a low-quality matrix (over land). Their long-term persistence requires a certain level of inter-population migration. Metapopulation species are vulnerable to habitat loss and fragmentation, and wetland species in particular may face insurmountable challenges of persisting in urbanized landscapes. By sampling two species across a large geographic area encompassing natural and urbanized landscapes, Homola and coauthors were able to tease apart differential effects of natural and anthropogenic landscape features on metapopulation dynamics.

They tested three specific hypotheses:

(1) Broadscale patterns of genetic structure should differ between the two species and should be scale dependent.

(2) Greater urbanization should increase population isolation and reduce genetic diversity, with differential effects of landscape features on the two species.

(3) Natural landscape features such as rivers and elevation should diminish gene flow across the landscape more strongly than anthropogenic features in general, but features of the most urbanized areas such as road density should be the strongest predictors of genetic isolation at local scales. 

urban amphibians
Fig. 1 from Homola et al. 2019 showing vernal pools in Maine where the authors sampled wood frogs and spotted salamanders over a 35,000 km2 region. Red background colors indicate greater urbanization, based on nighttime light intensity.

Isolated by distance

Wood frog
Wood frog, Lithobates sylvaticus, one of the two species sampled by Homola et al. (2019) in wetlands across Maine. Photo credit: Fralambert, Lithobates sylvaticus – Trois-Rivières, CC BY-SA 3.0

Homola and colleagues sampled a minimum of 10 individuals from each species per wetland and analyzed genetic diversity at 10 microsatellite loci. Their analysis of isolation by distance and genetic diversity supported their first hypothesis: the two species exhibit different patterns of isolation by distance (IBD) across the urban landscape, and these patterns are scale dependent.

Patterns of genetic isolation in spotted salamanders were strongly correlated with linear landscape distance. Genetic patterns in wood frogs, in contrast, exhibited a strong non-linear pattern. Isolation-by-distance was strongest at local spatial scales (<6km for wood frogs and <9km for spotted salamanders). The authors attribute the non-linear isolation-by-distance relationship in wood frogs to an absolute range boundary along one edge (the Atlantic Ocean), which could create a pattern of elevated genetic differentiation as fewer opportunities for immigration exist. They suggest that the observed pattern could also be attributable to patterns of post-glacial or post-deforestation recolonization and secondary contact in the region. Regardless of the mechanism, the two species have responded differentially to either the contemporary or historic processes that have shaped genetic connectivity across Maine. Moreover, the non-linear response of IBD in wood frogs and the scale-dependence effect of IBD in both species highlight that population genetics analyses are sensitive to the scale at which they are conducted.

Figure 2 from Homola et al. (2019): the two species sampled had contrasting geographic patterns of genetic diversity.

The effect of urbanization

Fig. 6 from Homola et al.: spotted salamanders and wood frogs both experience increasing genetic isolation in landscapes with more roads after accounting for the effects of isolation-by-distance.

A common pattern observed in other taxa is one of decreasing population connectivity and genetic diversity with increasing urbanization. Consistent with this pattern and supporting their second hypothesis, the authors found increased genetic isolation and decreased genetic diversity in both species associated with greater urbanization. Specifically, populations were more genetically isolated when occupying landscapes with large amounts of developed land cover and roads. These local-scale patterns demonstrate a clear negative impact of urbanization on genetic diversity and population connectivity in both species.

In general, the third hypothesis that natural features should impact genetic connectivity more strongly than the more recently arisen urban features was supported in wood frogs but not in spotted salamanders. At the landscape scale, the two species responded similarly to some, but not all, landscape features. Rivers strongly influenced wood frog populations, but not spotted salamander populations. In contrast, genetic isolation in both species was strongly associated with interstate highways, a surprising finding considering these barriers have only been present for ~60 years.

 

The differential effects of landscape features on gene flow that Homola and coauthors detected between two sympatric pond-breeding amphibians suggest that urban landscapes may reshape metapopulation dynamics in different ways for species sharing the same habitat. These findings highlight the need to study a variety of taxa in urban landscapes, even if they occupy similar habitat and share similar population dynamics. Patterns of genetic connectivity may be shaped by different historical processes of colonization and isolation with long-lasting impacts, but also reflect patterns of differential responses to contemporary barriers to gene flow such as roads. Their findings also highlight the importance of sampling metapopulations across broad geographic regions, as isolation-by-distance and landscape barriers may operate at distinct spatial scales that are species specific.

 


Read the full paper here:

Homola, J.J., Loftin, C.S. and Kinnison, M.T., 2019. Landscape genetics reveals unique and shared effects of urbanization for two sympatric pool‐breeding amphibians. Ecology and Evolution.

Featured photo credit:

Dave Huth from Allegany County, NY, USA, Spotted Sallie, Ambystoma maculatum (5739707713), CC BY 2.0

Kristin Winchell

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