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The role of hybridization during ecological divergence of southwestern white pine ( Pinus strobiformis ) and limber pine ( P. flexilis )

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Abstract

Interactions between extrinsic factors, such as disruptive selection, and intrinsic factors, such as genetic incompatibilities among loci, often contribute towards 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 P. flexilis. Utilizing ecological niche modeling, demographic modeling, 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 buildup of intrinsic incompatibilities and of co-adapted 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 strengths and directions of selection pressures across the long lifespans of conifers, in combination with their life history strategies, delay the evolution of strong intrinsic incompatibilities. This article is protected by copyright. All rights reserved.
https://www.biorxiv.org/content/biorxiv/ear
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... Analytical approaches have been developed to infer past demographic processes from population genomic data, which can now easily be generated even for conifers (Parchman et al. 2018). While many studies have used demographic inference to describe the phylogeographic history of a single species (e.g., Gugger et al. 2013;Li et al. 2013;Bagley et al. 2020;Ju et al. 2019;Park and Donoghue 2019;Capblancq et al. 2020;Yang et al. 2020;Labiszak et al. 2021), some of these established methods have also been used to infer divergence histories between two or three species (e.g., Zou et al. 2013;Christe et al. 2017;Kim et al. 2018;Menon et al. 2018). Single species inferences have found that the last glacial maximum (LGM; ~ 21 kya) affected distributional shifts and intraspecific gene flow dynamics, while multispecies studies have focused almost solely on how these climatic oscillations drove periods of increased and decreased interspecific gene flow which contributed to the formation of environmentally dependent hybrid zones, ancient and periodical introgression, or adaptive divergence in the development of reproductive isolation. ...
... Climate raster data (i.e., 19 bioclimatic variables at 30-arc-second resolutions), as well as elevational raster data from WorldClim, were extracted, as mentioned previously, from geographic coordinates for each sampled tree and then tested for correlation using Pearson's correlation coefficient (r). Five bioclimatic variables that are known to influence diversification in the genus Pinus (Jin et al. 2021;Menon et al. 2018), but that were also not highly correlated (r <|0.75|), were retained for analysis: mean diurnal range (Bio2), maximum temperature of the warmest quarter (Bio10), and minimum temperature of the coldest quarter (Bio11), precipitation seasonality (Bio15), and precipitation of the driest quarter (Bio17). The full explanatory data set included these five bioclimatic variables, latitude, longitude, and elevation. ...
... Paleoclimate raster data for the LGM (~ 21 kya) and Holocene (HOL, ~ 6 kya) were downloaded for three General Circulation Models (GCMs; CCSM4, MIROC-ESM, and MPI-ESM). Ensembles were built by averaging the habitat suitability predictions from the three GCMs for each time period (e.g., Menon et al. 2018). SDM predictions associated with each individual GCM, for both the HOL and LGM, were analyzed for incongruences as recommended in Varela et al. (2015). ...
Article
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Long-lived species of trees, especially conifers, often display weak patterns of reproductive isolation, but clear patterns of local adaptation and phenotypic divergence. Discovering the evolutionary history of these patterns is paramount to a generalized understanding of speciation for long-lived plants. We focus on two closely related yet phenotypically divergent pine species, Pinus pungens and P. rigida, that co-exist along high elevation ridgelines of the southern Appalachian Mountains. In this study, we performed historical species distribution modeling (SDM) to form hypotheses related to population size change and gene flow to be tested in a demographic inference framework. We further sought to identify drivers of divergence by associating climate and geographic variables with genetic structure within and across species boundaries. Population structure within each species was absent based on genome-wide RADseq data. Signals of admixture were present range-wide, however, and species-level genetic differences associated with precipitation seasonality and elevation. When combined with information from contemporary and historical species distribution models, these patterns are consistent with a complex evolutionary history of speciation influenced by Quaternary climate. This was confirmed using inferences based on the multidimensional site frequency spectrum, where demographic modeling inferred recurring gene flow since divergence (2.74 million years ago) and population size reductions that occurred during the last glacial period (~ 35.2 thousand years ago). This suggests that phenotypic and genomic divergence, including the evolution of divergent phenological schedules leading to partial reproductive isolation, as previously documented for these two species, can happen rapidly, even between long-lived species of pines.
... In the 1970s geneticists reported hybridization in Arizona between limber pine and SW white pine (Steinhoff and Andresen, 1971). Recently, the broad hybrid zone across the U.S. portion of the SW white pine's range has been confirmed using genomic tools (Moreno-Letelier & Piñero, 2009;Menon et al., 2018). For this discussion, we will refer to the U.S. and Mexican distributions as SW white pine, although ongoing research may lead to changes in the taxonomy (Fig. 2). ...
... R genes to C. ribicola are present in sugar pine (Cr1), western white pine (Cr2), SW white pine (Cr3), and limber pine (Cr4) (Kinloch and Dupper, 2002;. Emerging genomic research suggests that Cr3 and Cr4 may be the same or similar R gene in SW white pine and limber pine (Liu et al., , 2021, which may be explained by the historical natural hybridization of the two pine species (Menon et al., 2018). Because an R gene prevents disease development after infection (Kinloch and Dupper, 2002;, they increase the fitness of the host in the presence of C. ribicola. ...
... Depending on the North American Monsoon, drought conditions can persist into the fall. Studies of drought response of SW white pine in forests in the U.S. are complicated by the likelihood of including both SW white pine and hybrid SW white pine -limber pine individuals (Menon et al., 2018;Peach, 2021). Indications are that SW white pine has moderate drought tolerance but is less tolerant than limber pine (Waring, pers. ...
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Tree mortality rates have been increasing globally with mountainous regions experiencing higher temperatures and impacts from the expansion and intensification of pests and invasion by non-native agents. Western North American high-elevation forests exemplify these trends, and they often include one or more species of five-needle white pines (High-5 hereafter). These species share many characteristics critical to defining the structure and function of many subalpine forests. The main threats to High-5 populations include the non-native pathogen Cronartium ribicola, which causes the disease white pine blister rust, climate-driven drought stress, episodic and high mortality from mountain pine beetle (Dendroctonus ponderosae), and wildfires of increasing frequency, size, and intensity. The six High-5 species occurring in western North America (whitebark pine, Pinus albicaulis; limber pine, P. flexilis; southwestern white pine, P. strobiformis; Rocky Mountain bristlecone pine, P. aristata; Great Basin bristlecone pine, P. longaeva; and foxtail pine, P. balfouriana) differ in their health status and threat level. The convergence of threats impacting the rapidly declining species could portend future declines in the species and populations currently less impacted by recent disturbances. Differences in the innate adaptive capacities of the species affect their population trajectories under these novel combinations of stressors. We evaluate the status and outlook for each species and address the following questions: (1) Is the environment changing too fast and the intensity of stressors too great for the species to adapt and recover? (2) Do the species have the heritable traits necessary to sustain fitness under C. ribicola and climatic stresses? (3) Are other mortality factors increasing to the degree that they reduce the populations further and delay or preclude adaptation and population recovery? (4) Can the species escape the stressors through migration? Insights related to these questions provide guidance for forest management to facilitate adaptation and increase the resilience of these species into the future.
... Effective populations sizes of other pines have been estimated to be from a few dozens to a few thousand times greater than those inferred for island and mainland populations (Menon et al., 2018;Xia et al., 2018). The best fit demographic model predicted an ancestral effective population size (N A ) of 1124 and only a limited increase in population size following divergence. ...
... While identification of the appropriate effective population size necessary to protect adaptive evolutionary potential for rare species is still debated, recommendations generally range between 500 to 5000 individuals (Frankham et al., 2014;Franklin & Frankham, 1998;Lynch & Lande, 1998). Torrey pine, critically endangered and endemic to just two native populations, suffers from extremely low effective population size (N I = 2305, N M = 1715) relative to other pines (Menon et al., 2018;Xia et al., 2018). (Goto et al., 2011;Hufford & Mazer, 2003;Montalvo & Ellstrand, 2001). ...
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Understanding the contribution of neutral and adaptive evolutionary processes to population differentiation is often necessary for better informed management and conservation of rare species. In this study, we focused on Pinus torreyana Parry (Torrey pine), one of the world’s rarest pines, endemic to one island and one mainland population in California. Small population size, low genetic diversity, and susceptibility to abiotic and biotic stresses suggest Torrey pine may benefit from inter‐population genetic rescue to preserve the species’ evolutionary potential. We leveraged reduced representation sequencing to tease apart the respective contributions of stochastic and deterministic evolutionary processes to population differentiation. We applied these data to model spatial and temporal demographic changes in effective population sizes and genetic connectivity, to identify loci possibly under selection, and evaluate genetic rescue as a potential conservation strategy. Overall, we observed exceedingly low standing variation within both Torrey pine populations, reflecting consistently low effective population sizes across time, and limited genetic differentiation, suggesting maintenance of gene flow between populations following divergence. However, genome scans identified more than 2000 candidate SNPs potentially under divergent selection. Combined with previous observations indicating population phenotypic differentiation, this indicates natural selection has likely contributed to the evolution of population genetic differences. Thus, while reduced genetic diversity, small effective population size, and genetic connectivity between populations suggest genetic rescue could mitigate the adverse effects of rarity, evidence for adaptive differentiation suggests genetic mixing could disrupt adaptation. Further work evaluating the fitness consequences of inter‐population admixture is necessary to empirically evaluate the trade‐offs associated with genetic rescue in Torrey pine.
... An additional consideration for P. strobiformis and for the generalization of levels of genetic resistance across its range involves the position of its northern range within a moving hybrid zone with P. flexilis. Recent studies have found that the two species hybridize (Menon et al., 2018) and because P. flexilis is also known to have low levels of MGR (Schoettle et al., 2013), it is unclear if the somewhat higher level of resistance in P. strobiformis, relative to other white pines, is the product of introgression within this hybrid zone. One of the results of Menon et al. (2018) was that there was little ongoing gene flow between the periphery and core of the P. strobiformis range. ...
... Recent studies have found that the two species hybridize (Menon et al., 2018) and because P. flexilis is also known to have low levels of MGR (Schoettle et al., 2013), it is unclear if the somewhat higher level of resistance in P. strobiformis, relative to other white pines, is the product of introgression within this hybrid zone. One of the results of Menon et al. (2018) was that there was little ongoing gene flow between the periphery and core of the P. strobiformis range. The question then begs to be asked, will much of the species range outside of this hybrid zone be more susceptible to the advance of C. ribicola in the future? ...
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White pine blister rust, caused by the non-native, invasive fungal pathogen Cronartium ribicola, is a significant cause of mortality in white pines (Pinus subgenus Strobus) in North America. Along with climate-driven range contraction, mortality from blister rust can seriously impact the abundance and distribution of the nine white pine species native to the United States and Canada. Very little evaluation of this disease in southwestern white pine (Pinus strobiformis) has been previously undertaken, but genetic resistance to the disease has been documented, including major gene resistance (MGR) conferred by a dominant R gene. Data is emerging suggesting that the species also has quantitative disease resistance (QR). Our results suggest QR occurs at low frequency, with perhaps 10% of trees having a moderate level (> 35% survival). We assessed progeny arrays from 40 P. strobiformis families (1873 seedlings), originating from three populations, inoculated with C. ribicola. Subsequently, the seedlings were assessed for signs, symptoms and resulting impact in a common garden trial over a 7.5-year period to determine the types and frequency of resistance in a portion of this species’ range. There was a high incidence of both stem symptoms and mortality in the P. strobiformis families tested, and families ranged in survival from 0 to 84.6%. Three families had > 70% survival, representing perhaps the highest documented QR to date in a North American white pine species. Approximately 29.1% of the 441 surviving seedlings showed no stem symptoms, and of the approximately 70.8% of seedlings surviving with infections only few (24 of 316) had infections of moderate to high severity. QR traits associated with improved survival were primarily related to lower severity of infection, a reduced number of stem symptoms, and an increased number of bark reactions. Despite the high overall susceptibility, the presence of QR appears to be at a frequency and level useful to forest managers involved in restoration and reforestation efforts.
... MPB attacks have been observed on foxtail pine, although significantly fewer than on other pines growing in the same stand , Nesmith et al., 2019, Dudney et al., 2020. Similarly, in the introgression hybrid zone of southwestern white and limber pines in Arizona (Menon et al., 2018) isolated attacks and successful MPB reproduction occurs (McManis et al., 2018, although large scale MPB outbreaks in these forests have not been recorded. In an extensive survey across the range of another highelevation pine species, Great Basin bristlecone pine, no successful MPB attacks were found despite extensive MPB-caused mortality in cooccurring limber pine . ...
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... In the San Juan Mountain region, southwestern white pine is rarely dominant, rather is part of a complex mixture of tree species dominated by Douglas-fir (Looney and Waring 2013). Interestingly, southwestern white pine is also known to hybridize with limber pine in the San Juan Mountain region (Menon et al., 2018). ...
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Hybrid zones are a valuable tool for studying the process of speciation and for identifying the genomic regions undergoing divergence and the ecological (extrinsic) and non-ecological (intrinsic) factors involved. Here, we explored the genomic and geographic landscape of divergence in a hybrid zone between Papilio glaucus and Papilio canadensis. Using a genome scan of 28,417 ddRAD SNPs, we identified genomic regions under possible selection and examined their distribution in the context of previously identified candidate genes for ecological adaptations. We showed that differentiation was genome-wide, including multiple candidate genes for ecological adaptations, particularly those involved in seasonal adaptation and host plant detoxification. The Z-chromosome and four autosomes showed a disproportionate amount of differentiation, suggesting genes on these chromosomes play a potential role in reproductive isolation. Cline analyses of significantly differentiated genomic SNPs, and of species diagnostic genetic markers, showed a high degree of geographic coincidence (81%) and concordance (80%) and were associated with the geographic distribution of a climate-mediated developmental threshold (length of the growing season). A relatively large proportion (1.3%) of the outliers for divergent selection were not associated with candidate genes for ecological adaptations and may reflect the presence of previously unrecognized intrinsic barriers between these species. These results suggest that exogenous (climate-mediated) and endogenous (unknown) clines may have become coupled and act together to reinforce reproductive isolation. This approach of assessing divergence across both the genomic and geographic landscape can provide insight about the interplay between the genetic architecture of reproductive isolation and endogenous and exogenous selection. This article is protected by copyright. All rights reserved.
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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. This article is protected by copyright. All rights reserved.
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