Interactions between extrinsic factors, such as disruptive selection and intrinsic factors, such as genetic incompatibilities among loci, often contribute to the maintenance of species boundaries. The relative roles of these factors in the establishment of reproductive isolation can be examined using species pairs characterized by gene flow throughout their divergence history. We investigated the process of speciation and the maintenance of species boundaries between Pinus strobiformis and Pinus flexilis. Utilizing ecological niche modelling, demographic modelling and genomic cline analyses, we illustrated a divergence history with continuous gene flow. Our results supported an abundance of advanced generation hybrids and a lack of loci exhibiting steep transition in allele frequency across the hybrid zone. Additionally, we found evidence for climate-associated variation in the hybrid index and niche divergence between parental species and the hybrid zone. These results are consistent with extrinsic factors, such as climate, being an important isolating mechanism. A build-up of intrinsic incompatibilities and of coadapted gene complexes is also apparent, although these appear to be in the earliest stages of development. This supports previous work in coniferous species demonstrating the importance of extrinsic factors in facilitating speciation. Overall, our findings lend support to the hypothesis that varying strength and direction of selection pressures across the long lifespans of conifers, in combination with their other life history traits, delays the evolution of strong intrinsic incompatibilities.
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.
lis ia 69 of 80 Lind et al: Local adaptation of P. albicaulis 2 Running Title: Local adaptation of P. albicaulis 19 20 ABSTRACT 38 For populations exhibiting high levels of gene flow, the genetic architecture of fitness-related 39 traits is expected to be polygenic and underlain by many small-effect loci that covary across a 40 network of linked genomic regions. For most coniferous taxa, studies describing this 41 architecture have been limited to single-locus approaches, possibly leaving the vast majority of 42 the underlying genetic architecture undescribed. Even so, molecular investigations rarely search 43 for patterns indicative of an underlying polygenic basis, despite prior expectations for this signal.44 Here, using a polygenic perspective, we employ single and multilocus analyses of genome-wide 45 data (n = 116,231 SNPs) to describe the genetic architecture of adaptation within whitebark pine 46 (Pinus albicaulis Engelm.) across the local extent of the environmentally heterogeneous Lake ୗ = 0.0069) there is 48 strong evidence for polygenic adaptation to the rain shadow experienced across the eastern 49 Sierra Nevada. Specifically, we find little evidence for large-effect loci and that the frequencies 50 of loci associated with 4/5 phenotypes (mean = 236 SNPs), 18 environmental variables (mean = 51 99 SNPs), and those detected through genetic differentiation (n = 110 SNPs) exhibit 52 significantly higher covariance than random SNPs. We also provide evidence that this 53 covariance tracks environmental measures related to soil water availability through subtle allele 54 frequency shifts across populations. Our results provide replicative support for theoretical 55 expectations and highlight advantages of a polygenic perspective, as unremarkable loci when 56 viewed from a single-locus perspective are noteworthy when viewed through a polygenic lens, 57 particularly when considering protective measures such as conservation guidelines and 58 restoration strategies. Lind et al: Local adaptation of P. albicaulis 5 empirical (Hall et al. 2007; Luquez et al. 2007) investigations exploring the relationship between 86 phenotypic differentiation (e.g., Q ST ) and that of the underlying loci (e.g, G ST or F ST ) have shown 87 that discordance between these two structural indices can occur under adaptive evolution. 88Moreover, as the number of underlying loci increases, the divergence between these indices 89 increases as well, and the contribution of F ST to any individual underlying locus decreases. In 90 cases that exhibit strong diversifying selection and high gene flow, this adaptive divergence 91 results from selection on segregating genetic variation (Hermisson and Pennings 2005; Barret 92 and Schluter 2008) and is attributable to the between-population component of linkage 93 disequilibrium (Ohta 1982, Latta 1998). In the short term, local adaptation will be realized 94 through subtle coordinated shifts of allele frequencies across populations causing covariance 95
The European gypsy moth (Lymantria dispar L.) was first introduced to Massachusetts in 1869 and within 150 years has spread throughout eastern North America. This large‐scale invasion across a heterogeneous landscape allows examination of the genetic signatures of adaptation potentially associated with rapid geographical spread. We tested the hypothesis that spatially divergent natural selection has driven observed changes in three developmental traits that were measured in a common garden for 165 adult moths sampled from six populations across a latitudinal gradient covering the entirety of the range. We generated genotype data for 91,468 single nucleotide polymorphisms based on double digest restriction‐site associated DNA sequencing and used these data to discover genome‐wide associations for each trait, as well as to test for signatures of selection on the discovered architectures. Genetic structure across the introduced range of gypsy moth was low in magnitude (FST = 0.069), with signatures of bottlenecks and spatial expansion apparent in the rare portion of the allele frequency spectrum. Results from applications of Bayesian sparse linear mixed models were consistent with the presumed polygenic architectures of each trait. Further analyses indicated spatially divergent natural selection acting on larval development time and pupal mass, with the linkage disequilibrium component of this test acting as the main driver of observed patterns. The populations most important for these signals were two range‐edge populations established less than 30 generations ago. We discuss the importance of rapid polygenic adaptation to the ability of non‐native species to invade novel environments.
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