Spatial extent of analysis influences observed patterns of population genetic structure in a widespread darter species (Percidae)

Abstract

Connectivity among stream fish populations allows for exchange of genetic material and helps maintain genetic diversity, adaptive potential and population stability over time. Changes in species demographics and population connectivity have the potential to permanently alter the genetic patterns of stream fish, although these changes through space and time are variable and understudied in small‐bodied freshwater fish. As a spatially widespread, common species of benthic freshwater fish, the variegate darter (Etheostoma variatum) is a model species for documenting how patterns of genetic structure and diversity respond to increasing isolation due to large dams and how scale of study may shape our understanding of these patterns. We sampled variegate darters from 34 sites across their range in the North American Ohio River basin and examined how patterns of genetic structure and diversity within and between populations responded to historical population changes and dams within and between populations. Spatial scale and configuration of genetic structure varied across the eight identified populations, from tributaries within a watershed, to a single watershed, to multiple watersheds that encompass Ohio River mainstem habitats. This multiwatershed pattern of population structuring suggests genetic dispersal across large distances was and may continue to be common, although some populations remain isolated despite no apparent structural dispersal barriers. Populations with low effective population sizes and evidence of past population bottlenecks showed low allelic richness, but diversity patterns were not related to watershed size, a surrogate for habitat availability. Pairwise genetic differentiation (FST) increased with fluvial distance and was related to both historic and contemporary processes. Genetic diversity changes were influenced by underlying population size and stability, and while instream barriers were not strong determinants of genetic structuring or loss of genetic diversity, they reduce population connectivity and may impact long‐term population persistence. The broad spatial scale of this study demonstrated the large spatial extent of some variegate darter populations and indicated that dispersal is more extensive than expected given the movement patterns typically observed for small‐bodied, benthic fish. Dam impacts depended on underlying population size and stability, with larger populations more resilient to genetic drift and allelic richness loss than smaller populations. Other darters that inhabit large river habitats may show similar patterns in landscape‐scale studies, and large river barriers may impact populations of small‐bodied fish more than previously expected. Estimation of dispersal rates and behaviours is critical to conservation of imperilled riverine species such as darters.

Striking habitat reduction, decreased genetic diversity, and imperilled conservation of natural populations of Terrapenecoahuila

“…Changes in species demographics and population connectivity have the potential to permanently alter the genetic patterns of freshwater species, such as for instance in the variegate darter ( Etheostoma variatum ) inhabiting the Ohio river basin where dams have fragmented and isolated populations (Argentina et al., 2018). Hence, the maintenance of gene flow between populations is essential for the conservation of species, especially when they have small populations.…”

“…In addition, endemic species and those with small geographic range that have low dispersal abilities, frequently exhibit small population sizes and limited connectivity. Consequently, they may face stochastic genetic processes such as drift and inbreeding, and their populations may show low levels of genetic variability and be highly structured (Allendorf et al., 2013; Argentina et al., 2018; Sunny et al., 2014).…”

Genomic and phenotypic divergence informs translocation strategies for an endangered freshwater fish

“…In North American darters alone, some cases of genetic subdivision are associated with human impacts such as dams and habitat degradation (Beneteau et al, 2009;Blanton et al, 2019;Fluker et al, 2019;Haponski et al, 2007;Sterling et al, 2012). In other cases, population structure has emerged from isolation-by-distance or drainage discontinuity (Argentina et al, 2018;Euclide & Marsden, 2018).…”

“…In North American darters alone, some cases of genetic subdivision are associated with human impacts such as dams and habitat degradation (Beneteau et al, 2009; Blanton et al, 2019; Fluker et al, 2019; Haponski et al, 2007; Sterling et al, 2012). In other cases, population structure has emerged from isolation‐by‐distance or drainage discontinuity (Argentina et al, 2018; Euclide & Marsden, 2018). Darter ecology and reproductive behaviour may also play a key role in maintaining population structure, as these fishes can have strong preferences for specific microhabitats (Alexander & Phillips, 2012) and sexual traits (Williams & Mendelson, 2011).…”

“…For example, there is evidence that freshwater fish diversification and speciation has occurred within, as opposed to between, disjunct highland areas and river systems (Hollingsworth & Near, 2009; Keck & Near, 2010). Even within contiguous waterways, anthropogenic factors such as dams, reservoirs, and habitat fragmentation (e.g., Beneteau et al, 2009; Haponski et al, 2007; Yamamoto et al, 2004) can compound longer‐term evolutionary processes such as isolation‐by‐distance (e.g., Argentina et al, 2018; Zieritz et al, 2010) and result in genetic structure that varies between populations.…”