Genetic data improves niche model discrimination and alters the direction and magnitude of climate change forecasts.

Ecological niche models (ENMs) have classically operated under the simplifying assumptions that there are no barriers to gene flow, species are genetically homogeneous (i.e., no population-specific local adaptation), and all individuals share the same niche. Yet, these assumptions are violated for most broadly distributed species. Here, we incorporate genetic data from the widespread riparian tree species narrowleaf cottonwood (Populus angustifolia) to examine whether including intraspecific genetic variation can alter model performance and predictions of climate change impacts. We found that (1) P. angustifolia is differentiated into six genetic groups across its range from México to Canada and (2) different populations occupy distinct climate niches representing unique ecotypes. Comparing model discriminatory power, (3) all genetically informed ecological niche models (gENMs) outperformed the standard species-level ENM (3-14% increase in AUC; 1-23% increase in pROC). Furthermore, (4) gENMs predicted large differences among ecotypes in both the direction and magnitude of responses to climate change and (5) revealed evidence of niche divergence, particularly for the Eastern Rocky Mountain ecotype. (6) Models also predicted progressively increasing fragmentation and decreasing overlap between ecotypes. Contact zones are often hotspots of diversity that are critical for supporting species' capacity to respond to present and future climate change, thus predicted reductions in connectivity among ecotypes is of conservation concern. We further examined the generality of our findings by comparing our model developed for a higher elevation Rocky Mountain species with a related desert riparian cottonwood, P. fremontii. Together our results suggest that incorporating intraspecific genetic information can improve model performance by addressing this important source of variance. gENMs bring an evolutionary perspective to niche modeling and provide a truly "adaptive management" approach to support conservation genetic management of species facing global change.

Large effect quantitative trait loci for salicinoid phenolic glycosides in Populus: Implications for gene discovery.

Genomic studies have been used to identify genes underlying many important plant secondary metabolic pathways. However, genes for salicinoid phenolic glycosides (SPGs)-ecologically important compounds with significant commercial, cultural, and medicinal applications-remain largely undescribed. We used a linkage map derived from a full-sib population of hybrid cottonwoods (Populus spp.) to search for quantitative trait loci (QTL) for the SPGs salicortin and HCH-salicortin. SSR markers and primer sequences were used to anchor the map to the V3.0 P. trichocarpa genome. We discovered 21 QTL for the two traits, including a major QTL for HCH-salicortin (R2 = .52) that colocated with a QTL for salicortin on chr12. Using the V3.0 Populus genome sequence, we identified 2,983 annotated genes and 1,480 genes of unknown function within our QTL intervals. We note ten candidate genes of interest, including a BAHD-type acyltransferase that has been potentially linked to Populus SPGs. Our results complement other recent studies in Populus with implications for gene discovery and the evolution of defensive chemistry in a model genus. To our knowledge, this is the first study to use a full-sib mapping population to identify QTL intervals and gene lists associated with SPGs.

Conserving threatened riparian ecosystems in the American West: Precipitation gradients and river networks drive genetic connectivity and diversity in a foundation riparian tree (Populus angustifolia).

Gene flow is an evolutionary process that supports genetic connectivity and contributes to the capacity of species to adapt to environmental change. Yet, for most species, little is known about the specific environmental factors that influence genetic connectivity, or their effects on genetic diversity and differentiation. We used a landscape genetic approach to understand how geography and climate influence genetic connectivity in a foundation riparian tree (Populus angustifolia), and their relationships with specieswide patterns of genetic diversity and differentiation. Using multivariate restricted optimization in a reciprocal causal modelling framework, we quantified the relative contributions of riparian network connectivity, terrestrial upland resistance and climate gradients on genetic connectivity. We found that (i) all riparian corridors, regardless of river order, equally facilitated connectivity, while terrestrial uplands provided 2.5× more resistance to gene flow than riparian corridors. (ii) Cumulative differences in precipitation seasonality and precipitation of the warmest quarter were the primary climatic factors driving genetic differentiation; furthermore, maximum climate resistance was 45× greater than riparian resistance. (iii) Genetic diversity was positively correlated with connectivity (R2  = 0.3744, p = .0019), illustrating the utility of resistance models for identifying landscape conditions that can support a species' ability to adapt to environmental change. From these results, we present a map highlighting key genetic connectivity corridors across P. angustifolia's range that if disrupted could have long-term ecological and evolutionary consequences. Our findings provide recommendations for conservation and restoration management of threatened riparian ecosystems throughout the western USA and the high biodiversity they support.

Climate relicts and their associated communities as natural ecology and evolution laboratories.

Climate relicts, marginal populations that have become isolated via climate-driven range shifts, preserve ecological and evolutionary histories that can span millennia. Studies point to climate relicts as 'natural laboratories' for investigating how long-term environmental change impacts species and populations. However, we propose that such research should be expanded to reveal how climate change affects 'interacting' species in ways that reshape community composition and evolution. Biotic interactions and their community and ecosystem effects are often genetically based and driven by associations with foundation species. We discuss evolution in climate relicts within the context of the emerging fields of community and ecosystem genetics, exploring the idea that foundation relicts are also natural community and ecosystem laboratories and windows to future landscapes.

Tree hybridization and genotypic variation drive cryptic speciation of a specialist mite herbivore.

Few studies have investigated the roles that plant hybridization and individual plant genotype play in promoting population divergence within arthropod species. Using nrDNA sequence information and reciprocal transfer experiments, we examined how tree cross type (i.e., pure Populus angustifolia and P. angustifolia x P. fremontii F(1) type hybrids) and individual tree genotype influence host race formation in the bud-galling mite Aceria parapopuli. Three main findings emerged: (1) Strong genetic differentiation of mite populations found on pure P. angustifolia and F(1) type hybrids indicates that these mites represent morphologically cryptic species. (2) Within the F(1) type hybrids, population genetic analyses indicate migration among individual trees; however, (3) transfer experiments show that the mites found on heavily infested F(1) type trees perform best on their natal host genotype, suggesting that genetic interactions between mites and their host trees drive population structure, local adaptation, and host race formation. These findings argue that hybridization and genotypic differences in foundation tree species may drive herbivore population structure, and have evolutionary consequences for dependent arthropod species.

Lack of genetic differentiation in aggressive and secondary bark beetles (Coleoptera: Curculionidae, Scolytinae) from Arizona.

Bark beetles (Coleoptera: Curculionidae, Scolytinae) play an important role as disturbance agents in ponderosa pine (Pinus ponderosa Douglas ex Lawson) forests of Arizona. However, from 2001 to 2003, elevated bark beetle activity caused unprecedented levels of ponderosa pine mortality. A better understanding of the population structure of these species will facilitate analysis of their dispersal patterns and improve management strategies. Here, we use fluorescently labeled amplified fragment length polymorphism (fAFLP) analysis to resolve genetic variation among and within sampling locations in northcentral Arizona of Ips pini (Say), Dendroctonus brevicomis LeConte, and D. frontalis Zimmermann. We generated genetic fingerprints for >500 beetle specimens and analyzed genetic diversity. For all species, gene flow estimates among sampling locations were high, and significant population subdivision was not discernible across a large portion of ponderosa pine forests in Arizona. However, a weak relationship was detected with I. pini population structure and elevation. Because of the lack of genetic differentiation detected throughout the large study area, our findings suggest these insects are capable of long distance dispersal and exhibit a high degree of gene flow across a broad region. We conclude that our results are consistent with strong dispersal patterns and large population sizes of all three species.

Extending genomics to natural communities and ecosystems.

An important step in the integration of ecology and genomics is the progression from molecular studies of relatively simple model systems to complex field systems. The recent availability of sequenced genomes from key plants is leading to a new understanding of the molecular drivers of community composition and ecosystem processes. As genome sequences accumulate for species that form intimate associations in nature, a detailed view may emerge as to how these associations cause changes among species at the nucleotide level. This advance could dramatically alter views about the structure and evolution of communities and ecosystems.

Genome structure and emerging evidence of an incipient sex chromosome in Populus.

The genus Populus consists of dioecious woody species with largely unknown genetic mechanisms for gender determination. We have discovered genetic and genomic features in the peritelomeric region of chromosome XIX that suggest this region of the Populus genome is in the process of developing characteristics of a sex chromosome. We have identified a gender-associated locus that consistently maps to this region. Furthermore, comparison of genetic maps across multiple Populus families reveals consistently distorted segregation within this region. We have intensively characterized this region using an F(1) interspecific cross involving the female genotype that was used for genome sequencing. This region shows suppressed recombination and high divergence between the alternate haplotypes, as revealed by dense map-based genome assembly using microsatellite markers. The suppressed recombination, distorted segregation, and haplotype divergence were observed only for the maternal parent in this cross. Furthermore, the progeny of this cross showed a strongly male-biased sex ratio, in agreement with Haldane's rule that postulates that the heterogametic sex is more likely to be absent, rare, or sterile in interspecific crosses. Together, these results support the role of chromosome XIX in sex determination and suggest that sex determination in Populus occurs through a ZW system in which the female is the heterogametic gender.