Water availability drives signatures of local adaptation in whitebark pine (Pinus albicaulis Engelm.) across fine spatial scales of the Lake Tahoe Basin, USA

Abstract

Patterns of local adaptation at fine spatial scales are central to understanding how evolution proceeds, and are essential to the effective management of economically and ecologically important forest tree species. Here, we employ single and multilocus analyses of genetic data (n = 116 231 SNPs) to describe signatures of fine‐scale adaptation within eight whitebark pine (Pinus albicaulis Engelm.) populations across the local extent of the environmentally heterogeneous Lake Tahoe Basin, USA. We show that despite highly shared genetic variation (FST = 0.0069), there is strong evidence for adaptation to the rain shadow experienced across the eastern Sierra Nevada. Specifically, we build upon evidence from a common garden study and find that allele frequencies of loci associated with four phenotypes (mean = 236 SNPs), 18 environmental variables (mean = 99 SNPs), and those detected through genetic differentiation (n = 110 SNPs) exhibit significantly higher signals of selection (covariance of allele frequencies) than could be expected to arise, given the data. We also provide evidence that this covariance tracks environmental measures related to soil water availability through subtle allele frequency shifts across populations. Our results replicate empirical support for theoretical expectations of local adaptation for populations exhibiting strong gene flow and high selective pressures and suggest that ongoing adaptation of many P. albicaulis populations within the Lake Tahoe Basin will not be constrained by the lack of genetic variation. Even so, some populations exhibit low levels of heritability for the traits presumed to be related to fitness. These instances could be used to prioritize management to maintain adaptive potential. Overall, we suggest that established practices regarding whitebark pine conservation be maintained, with the additional context of fine‐scale adaptation.

Genomic and phenotypic divergence unveil microgeographic adaptation in the Amazonian hyperdominant tree Eperua falcata Aubl. (Fabaceae)

“…Data on perennial plants, and on trees in particular, suggest that this may be a general phenomenon, that can be readily observed at the phenotypic level (Yeaman and Jarvis 2006;Brousseau et al 2013;Vizcaíno-Palomar et al 2014;Lind et al 2017) (but see Latreille & Pichot (2017) for a case of complete lack of microgeographical adaptation) . At the molecular level, association between alleles (or genotypes) and habitats has been detected in a variety of cases (Cobb et al 1994;Mitton et al 1998;Kelly et al 2003;Jump et al 2006;Pluess and Weber 2012;Audigeos et al 2013;Csilléry et al 2014;Brousseau et al 2015;Eckert et al 2015;Lind et al 2017), which led us to a reconsideration of the adaptive role of intra-specific and intra-populational variation (Scotti et al 2016) .…”

“…At the molecular level, association between alleles (or genotypes) and habitats has been detected in a variety of cases (Cobb et al 1994;Mitton et al 1998;Kelly et al 2003;Jump et al 2006;Pluess and Weber 2012;Audigeos et al 2013;Csilléry et al 2014;Brousseau et al 2015;Eckert et al 2015;Lind et al 2017), which led us to a reconsideration of the adaptive role of intra-specific and intra-populational variation (Scotti et al 2016) . The advent of genomewide approaches has increased detection power, making it possible to more precisely evaluate the genetic bases of microgeographic adaptation (Turner et al 2010;Eckert et al 2015;Izuno All rights reserved.…”

“…http://dx.doi.org/10.1101/312843 doi: bioRxiv preprint first posted online Fustier et al 2017;Lind et al 2017). In general, those genome scan studies have found only a minority of loci (in the order of few percent) to be submitted to microgeographic disruptive selection.…”

“…Rather, outliers were specific to one spatial scale, suggesting that different portions of the genome respond to different types of environmental constraints; in future studies, local adaptation in wild populations should be reconsidered by integrating different spatial scales, including microgeographic habitat patchiness. It is however important to stress that our Bayesian approach may miss footprints of polygenic adaptation, if adaptation acts in different ways in the two study sites (through different selection strengths and/or different loci affected), even more in case of weak selection strength at many SNPs (Brousseau et al 2016), which is known to be common in nature (Berg and Coop 2014;Lind et al 2017;Harrisson et al 2017).…”

“…http://dx.doi.org/10.1101/312843 doi: bioRxiv preprint first posted online May. 2, 2018; 1 5 florida (Cornaceae) (Pais et al 2017), to aluminum and phosphate ion concentrations in Pinus contorta (Pinaceae) (Eckert et al 2012), to substrate age in Metrosideros polymorpha (Myrtaceae) (Izuno et al 2017), to soil types in Abies religiosa (Pinaceae) (Méndez-González et al 2017), or to soil water availability in Pinus albicaulis (Pinaceae) (Lind et al 2017).…”