Nuclear and chloroplast DNA phylogeography reveals high genetic diversity and postglacial range expansion in Quercus mexicana.

PREMISE: Phylogeographical studies are fundamental for understanding factors that influence the spatial distribution of genetic lineages within species. Population expansions and contractions, distribution shifts, and climate changes are among the most important factors shaping the genetic compositions of populations. METHODS: We investigated the phylogeography of an endemic oak, Quercus mexicana (Fagaceae), which has a restricted distribution in northeastern Mexico along the Sierra Madre Oriental and adjacent areas. Nuclear and chloroplast DNA microsatellite markers were used to describe the genetic diversity and structure of 39 populations of Q. mexicana along its entire distribution area. We tested whether population expansion or contraction events influenced the genetic diversity and structure of the species. We also modeled the historical distributional range of Q. mexicana (for the Mid Holocene, the Last Glacial Maximum, and the Last Interglacial) to estimate the extent to which climate fluctuations have impacted the distribution of this oak species. RESULTS: Our results revealed high genetic diversity and low genetic structure in Q. mexicana populations. Ecological niche models suggested historical fluctuations in the distributional range of Q. mexicana. Historical range changes, gene flow, and physical barriers seem to have played an important role in shaping the phylogeographic structure of Q. mexicana. CONCLUSIONS: Our study indicates that the genetic structure of Q. mexicana may have been the result of responses of oak trees not only to heterogeneous environments present in the Sierra Madre Oriental and adjacent areas, but also to elevational and latitudinal shifts in response to climate changes in the past.

Response to: A paleoecological context to assess the development of oak forest in Colombia: A comment on Zorrilla-Azcué, S., González-Rodríguez, A., Oyama, K., González, M.A. & Rodríguez-Correa, H., The DNA history of a lonely oak: Quercus humboldtii phylogeography in the Colombian Andes. Ecology and Evolution 2021, doi:10.1002/ece3.7529.

In this response, we address comments and clarify the rationale behind the choice of hypotheses aimed to describe the Quercus humboldtii phylogeography in the Colombian Andes. Finally, we explain our disagreement with the conclusions of a previous critique, since these are not necessarily adequate under the implemented population genetics approach.

The DNA history of a lonely oak: Quercus humboldtii phylogeography in the Colombian Andes.

The climatic and geological changes that occurred during the Quaternary, particularly the fluctuations during the glacial and interglacial periods of the Pleistocene, shaped the population demography and geographic distribution of many species. These processes have been studied in several groups of organisms in the Northern Hemisphere, but their influence on the evolution of Neotropical montane species and ecosystems remains unclear. This study contributes to the understanding of the effect of climatic fluctuations during the late Pleistocene on the evolution of Andean mountain forests. First, we describe the nuclear and plastidic DNA patterns of genetic diversity, structure, historical demography, and landscape connectivity of Quercus humboldtii, which is a typical species in northern Andean montane forests. Then, these patterns were compared with the palynological and evolutionary hypotheses postulated for montane forests of the Colombian Andes under climatic fluctuation scenarios during the Quaternary. Our results indicated that populations of Q. humboldtii have high genetic diversity and a lack of genetic structure and that they have experienced a historical increase in connectivity from the last glacial maximum (LGM) to the present. Furthermore, our results showed a dramatic reduction in the effective population size followed by an expansion before the LGM, which is consistent with the results found by palynological studies, suggesting a change in dominance in Andean forests that may be related to ecological factors rather than climate change.

High genetic diversity and stable Pleistocene distributional ranges in the widespread Mexican red oak Quercus castanea Née (1801) (Fagaceae).

The Mexican highlands are areas of high biological complexity where taxa of Nearctic and Neotropical origin and different population histories are found. To gain a more detailed view of the evolution of the biota in these regions, it is necessary to evaluate the effects of historical tectonic and climate events on species. Here, we analyzed the phylogeographic structure, historical demographic processes, and the contemporary period, Last Glacial Maximum (LGM) and Last Interglacial (LIG) ecological niche models of Quercus castanea, to infer the historical population dynamics of this oak distributed in the Mexican highlands. A total of 36 populations of Q. castanea were genotyped with seven chloroplast microsatellite loci in four recognized biogeographic provinces of Mexico: the Sierra Madre Occidental (western mountain range), the Central Plateau, the Trans-Mexican Volcanic Belt (TMVB, mountain range crossing central Mexico from west to east) and the Sierra Madre del Sur (SMS, southern mountain range). We obtained standard statistics of genetic diversity and structure and tested for signals of historical demographic expansions. A total of 90 haplotypes were identified, and 29 of these haplotypes were restricted to single populations. The within-population genetic diversity was high (mean h S = 0.72), and among-population genetic differentiation showed a strong phylogeographic structure (N ST = 0.630 > G ST = 0.266; p < .001). Signals of demographic expansion were identified in the TMVB and the SMS. The ecological niche models suggested a considerable percentage of stable distribution area for the species during the LGM and connectivity between the TMVB and the SMS. High genetic diversity, strong phylogeographic structure, and ecological niche models suggest in situ permanence of Q. castanea populations with large effective population sizes. The complex geological and climatic histories of the TMVB help to explain the origin and maintenance of a large proportion of the genetic diversity in this oak species.

Genomic landscape of the global oak phylogeny.

The tree of life is highly reticulate, with the history of population divergence emerging from populations of gene phylogenies that reflect histories of introgression, lineage sorting and divergence. In this study, we investigate global patterns of oak diversity and test the hypothesis that there are regions of the oak genome that are broadly informative about phylogeny. We utilize fossil data and restriction-site associated DNA sequencing (RAD-seq) for 632 individuals representing nearly 250 Quercus species to infer a time-calibrated phylogeny of the world's oaks. We use a reversible-jump Markov chain Monte Carlo method to reconstruct shifts in lineage diversification rates, accounting for among-clade sampling biases. We then map the > 20 000 RAD-seq loci back to an annotated oak genome and investigate genomic distribution of introgression and phylogenetic support across the phylogeny. Oak lineages have diversified among geographic regions, followed by ecological divergence within regions, in the Americas and Eurasia. Roughly 60% of oak diversity traces back to four clades that experienced increases in net diversification, probably in response to climatic transitions or ecological opportunity. The strong support for the phylogeny contrasts with high genomic heterogeneity in phylogenetic signal and introgression. Oaks are phylogenomic mosaics, and their diversity may in fact depend on the gene flow that shapes the oak genome.

Landscape genomics provides evidence of climate-associated genetic variation in Mexican populations of Quercus rugosa.

Local adaptation is a critical evolutionary process that allows plants to grow better in their local compared to non-native habitat and results in species-wide geographic patterns of adaptive genetic variation. For forest tree species with a long generation time, this spatial genetic heterogeneity can shape the ability of trees to respond to rapid climate change. Here, we identify genomic variation that may confer local environmental adaptations and then predict the extent of adaptive mismatch under future climate as a tool for forest restoration or management of the widely distributed high-elevation oak species Quercus rugosa in Mexico. Using genotyping by sequencing, we identified 5,354 single nucleotide polymorphisms (SNPs) genotyped from 103 individuals across 17 sites in the Trans-Mexican Volcanic Belt, and, after controlling for neutral genetic structure, we detected 74 F ST outlier SNPs and 97 SNPs associated with climate variation. Then, we deployed a nonlinear multivariate model, Gradient Forests, to map turnover in allele frequencies along environmental gradients and predict areas most sensitive to climate change. We found that spatial patterns of genetic variation were most strongly associated with precipitation seasonality and geographic distance. We identified regions of contemporary genetic and climatic similarities and predicted regions where future populations of Q. rugosa might be at risk due to high expected rate of climate change. Our findings provide preliminary details for future management strategies of Q. rugosa in Mexico and also illustrate how a landscape genomic approach can provide a useful tool for conservation and resource management strategies.

Contrasting Patterns of Population History and Seed-mediated Gene Flow in Two Endemic Costa Rican Oak Species.

Lower Central America is an important area to study recent population history and diversification of Neotropical species due to its complex and dynamic geology and climate. Phylogeographic studies in this region are few in comparison with other regions and even less for tree species. The aim of the present study was to characterize the phylogeographic structure in 2 partially co-distributed endemic oak species (Quercus costaricensis and Q. bumelioides) of the Costa Rican mountains using chloroplast short sequence repeats (cpSSRs), and to test for the effect of geological and palaeoclimatic processes on their population history. Genetic diversity and structure, haplotype networks, patterns of seed-mediated gene flow and historical demography were estimated for both species. Results suggested contrasting patterns. Quercus costaricensis exhibited high values of genetic diversity, a marked phylogeographic structure, a north-to-south genetic diversity gradient and evidence of a demographic expansion during the Quaternary. Quercus bumelioides did not show significant genetic structure and the haplotype network and historical demography estimates suggested a recent population expansion probably during the Pleistocene-Holocene transition. The phylogeographic structure of Q. costaricensis seems to be related to Pleistocene altitudinal migration due to its higher altitudinal distribution. Meanwhile, historical seed-mediated gene flow through the lower altitudinal distribution of Q. bumelioides may have promoted the homogenization of genetic variation. Population expansion and stable availability of suitable climatic areas in both species probably indicate that palaeoclimatic changes promoted downwards altitudinal migration and formation of continuous forests allowing oak species to expand their distribution into the Panamanian mountains during glacial stages.

Southward Pleistocene migration of Douglas-fir into Mexico: phylogeography, ecological niche modeling, and conservation of 'rear edge' populations.

• Poleward Pleistocene plant migration has been an important process structuring modern temperate and boreal plant communities, but the contribution of equatorward migration remains poorly understood. Paleobotanical evidence suggests Miocene or Pleistocene origin for temperate 'sky island' plant taxa in Mexico. These 'rear edge' populations situated in a biodiversity hotspot may be an important reserve of genetic diversity in changing climates. • We used mtDNA sequences, cpDNA sequences and chloroplast microsatellites to test hypotheses of Miocene vs Pleistocene colonization of temperate Douglas-fir in Mexico, explore geographic patterns of molecular variation in relation to Pleistocene climate history using ecological niche models, and assess the taxonomic and conservation implications. • We found strong evidence for Pleistocene divergence of Douglas-fir in Mexico (958 thousand yr before present (ka) with the 90% highest posterior density interval ranging from 1.6 million yr before present (Ma) to 491 ka), consistent with the southward Pleistocene migration hypothesis. Genetic diversity was high and strongly partitioned among populations. Spatial patterns of molecular variation and ecological niche models suggest a complex late Pleistocene history involving periods of isolation and expansion along mountain corridors. • These results highlight the importance of southward Pleistocene migration in establishing modern high-diversity plant communities and provide critical insights into proposals to conserve the unique biodiversity of Mexican Douglas-fir and associated taxa.