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Demographic Modeling Informs Functional Connectivity and Management Interventions in Graham’S Beardtongue

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Demographic Modeling Informs Functional Connectivity and Management Interventions in Graham’S Beardtongue Conservation Genetics https://doi.org/10.1007/s10592-021-01392-9 RESEARCH ARTICLE Demographic modeling informs functional connectivity and management interventions in Graham’s beardtongue Matthew R. Jones1 · Daniel E. Winkler2 · Rob Massatti1 Received: 16 December 2020 / Accepted: 30 July 2021 © The Author(s) 2021 Abstract Functional connectivity (i.e., the movement of individuals across a landscape) is essential for the maintenance of genetic vari- ation and persistence of rare species. However, illuminating the processes infuencing functional connectivity and ultimately translating this knowledge into management practice remains a fundamental challenge. Here, we combine various population structure analyses with pairwise, population-specifc demographic modeling to investigate historical functional connectivity in Graham’s beardtongue (Penstemon grahamii), a rare plant narrowly distributed across a dryland region of the western US. While principal component and population structure analyses indicated an isolation-by-distance pattern of diferentiation across the species’ range, spatial inferences of efective migration exposed an abrupt shift in population ancestry near the range center. To understand these seemingly conficting patterns, we tested various models of historical gene fow and found evidence for recent admixture (~ 3400 generations ago) between populations near the range center. This historical perspective reconciles population structure patterns and suggests management eforts should focus on maintaining connectivity between these previously isolated lineages to promote the ongoing transfer of genetic variation. Beyond providing species-specifc knowledge to inform management options, our study highlights how understanding demographic history may be critical to guide conservation eforts when interpreting population genetic patterns and inferring functional connectivity. Keywords Conservation · Genomics · Habitat fragmentation · Landscape genetics · Migration · Penstemon grahamii Introduction functional connectivity (i.e., the movement of individuals and genes across the landscape; Crooks & Sanjayan, 2006) Intensifying interactions between habitat destruction and between populations of rare species in the face of increasing climate change are a major threat to the persistence of many habitat fragmentation is therefore essential for the conserva- native species across the globe (Travis 2004; Mantyka- tion of biodiversity (Allendorf et al. 2012). Pringle et al. 2012). As these processes fragment a species’ The expanding accessibility of genome sequencing tech- range, isolated populations may experience stronger genetic nologies and analytical tools has greatly facilitated studies drift and inbreeding, leading to the loss of genetic diver- of functional connectivity and gene fow across a diverse sity and increasing the chance of local extinction over time array of rare, threatened, and ecologically important species (Wright 1931; Allendorf et al. 2012). Species with geneti- (Manel and Holderegger 2013). However, inferring patterns cally diverse and interconnected populations are likely more of gene fow from genomic data remains a fundamental chal- resilient to environmental change (Fisher 1930; Sgro et al. lenge in population genetics and landscape genetics (Cruick- 2011) and may ultimately contribute to more stable com- shank and Hahn 2014; Richardson et al. 2016; Beichman munities and ecosystems (Hughes et al. 2008). Maintaining et al. 2018). The challenge stems largely from the similar genetic patterns that may be produced by multiple demo- * Rob Massatti graphic and ecological processes (e.g., see Lawson et al., [email protected] 2018; Meirmans, 2012). For instance, regions of a species’ range marked by relatively sharp transitions in genetic difer- 1 U.S. Geological Survey, Southwest Biological Science entiation may occur when current gene fow is restricted by Center, Flagstaf, AZ, USA environmental gradients (Manthey and Moyle 2015; Weber 2 U.S. Geological Survey, Southwest Biological Science et al. 2017), physical barriers (e.g., mountain ranges, rivers, Center, Moab, UT, USA Vol.:(0123456789)1 3 Conservation Genetics or roads; Frantz et al., 2012), or poor habitat quality or habi- with proposals to list the species as endangered or threatened tat disturbance (Williams et al. 2003). Often, spatial patterns under the US Endangered Species Act in 1975, 1990, 2002, of genetic diferentiation are correlated with landscape-level 2006, and 2013 (US Fish and Wildlife Service 2005, 2020). variables to infer putative ecological mechanisms shaping To inform ongoing conservation eforts, there is a pressing connectivity (i.e., landscape genetics; Manel et al. 2003). need to characterize genetic diversity and infer connectivity However, a central assumption of many correlative land- across the species’ range. scape genetics approaches is that contemporary patterns Here, we performed double-digest restriction site-asso- of genetic variation refect a historical equilibrium of gene ciated DNA sequencing (ddRADseq) to investigate range- fow and genetic drift (Manel and Holderegger 2013), an wide patterns of genetic diversity and functional connec- assumption that may be seldom met in species with recently tivity in P. grahamii. First, to understand broad patterns of fragmented ranges (Whitlock and McCauley 1999). If the genetic structure refecting historical gene fow across the strength of gene fow or genetic drift has changed through range, we characterized the spatial distribution of genetic time (e.g., recent dispersal barriers or admixture between variation using principal component and population struc- previously isolated lineages), then traditional landscape ture analyses. Then, to more precisely understand the his- genetic inferences may be confounded (Landguth et al. 2010; torical demographic factors shaping these spatial patterns Epps and Keyghobad 2015). Understanding population his- of genetic diversity and population structure we modeled tory (i.e., demographic history) is therefore crucial for deter- the history of divergence, gene fow, and population size mining whether particular regions of a species’ range war- between P. grahamii lineages. Specifcally, we were inter- rant focused management actions to increase connectivity ested in testing whether P. grahamii lineages have expe- (Epps and Keyghobad 2015). rienced recent histories of isolation or secondary contact, Graham’s beardtongue (Penstemon grahamii D.D. Keck; which might infuence the interpretation of recent gene fow Plantaginaceae) is a rare perennial forb endemic to the Uinta based on population structure patterns. Our study provides Basin of eastern Utah and western Colorado. Populations valuable insights into functional connectivity of P. grahamii are patchily distributed across the oil shale-rich Green River and highlights important and often overlooked challenges formation, but the species is relatively common where it in elucidating the timing of gene fow from genomic data in occurs (total population census estimate of 56,385 indi- species of conservation concern. Specifcally, this research viduals across 9585 acres of occupied habitat; U.S. Fish reinforces the idea that correct interpretation of contempo- and Wildlife Service 2020). P. grahamii is adapted to xeric rary genetic patterns frst necessitates knowledge of histori- environments (annual precipitation ~ 6–12 inches) and adult cal demographic processes. plants appear capable of going into dormancy during excep- tionally dry conditions, which may facilitate its long-term persistence (U.S. Fish and Wildlife Service 2020). Within Methods a year, temperatures can vary substantially across its range, with average summer highs reaching approximately 34 °C Sample collection, DNA isolation and library (~ 93°F) and average winter lows of − 14 °C (~ 7°F). P. gra- preparation hamii seeds are primarily gravity- or wind-dispersed and pollinators include bees, wasps, and occasionally humming- To obtain representative samples spanning the distribu- birds. Pollination is believed to be crucial to the reproductive tion of P. grahamii, we visited the 27 Element Occurrences success of P. grahamii, yet it remains unclear whether dis- (EOs) of P. grahamii defned by the U.S. Fish and Wildlife persal and pollination are sufcient for maintaining genetic Service (U.S. Fish and Wildlife Service 2020) during the variation across its range. summer of 2019. Here, EOs are defned as occupied habi- Penstemon grahamii faces numerous threats from energy tats separated from other occupied habitats by at least 2 km development, mining, of-road vehicle use, and livestock (km) (U.S. Fish and Wildlife Service 2020). Plants were disturbance. Energy development is particularly threaten- found at 11 EOs across 22 individual sites and leaf tissues ing, as half of known P. grahamii occurrences and 5 of 6 of were sampled from 2 to 11 plants at each site (average 8.7 its largest occurrences are on lands currently leased for oil individuals per site, 192 individuals total; Supplementary and gas exploration (US Fish and Wildlife Service 2005). Table 1) separated from one another by at least 5 m to avoid Individuals are also relatively long-lived (up to 10 years) sampling close relatives. and populations may have low recruitment (US Fish and We extracted genomic DNA using DNeasy 96 Plant Kits Wildlife Service 2005), which naturally limits their ability (Qiagen, Germantown, MD, USA) following the manufac- to recover from disturbances
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