Juan Pablo Jaramillo-Correa

The genus Abies Mill. (Pinaceae) comprises a group of conifers distributed across boreal and temperate regions, including eight species with disjunct distributions across Mexico's highest mountain chains. Abies religiosa (Kunth) Schltdl. & Cham. is a dominant species of the Trans-Mexican Volcanic Belt in central Mexico, forming forests crucial for water retention, carbon sequestration, and soil stabilization. Despite its ecological importance, peri-urban forests dominated by this species around Mexico City are exposed to high levels of tropospheric ozone, which cause premature senescence and forest decline. Here, we report a saturated linkage map for A. religiosa generated by genotyping 182 megagametophytes from two mother trees for 9,702 single nucleotide polymorphisms. The linkage map is composed of 12 linkage groups (LGs) containing between 518 and 1,207 markers and spanning 1,567.88 cM (114 to 208 cM per LG). Annotation of reads containing SNPs allowed us to locate 5,881 coding genes on the map, of which 1,952 had known functions in conifers. Differential expression analyses of these genes in symptomatic and asymptomatic trees growing in a peri-urban forest heavily affected by ozone pollution revealed eight genes that were differentially expressed when ozone levels increased. Co-expression analyses further showed that neighboring genes tended to co-express more often in symptomatic than in asymptomatic trees, especially in clusters within LGs 5, 8, and 10. Gene pairs within co-expression clusters coded for similar proteins, suggesting functional co-localization. Our integrated approach reveals previously uncharacterized metabolic and defense pathways associated with ozone tolerance in conifers and lays the groundwork for developing molecular-based management programs accounting for ozone resistance in peri-urban forests.

Migration is a widespread phenomenon in animals that involves the synchronized movement of numerous individuals across habitats. While migratory traits appear to be environmentally triggered, evidence also points to a still poorly understood genetically regulated mechanism. The study of both the genomic architecture of migration and the degree of similarity across migrating taxa is a recurrent topic in evolutionary biology. Here, we investigated the genomic basis of migration in a flying mammal, the lesser long-nosed bat (Leptonycteris yerbabuenae), a nectar-feeding bat with a partially migratory behavior. Each year, the migrant group of females travels north from central Mexico to give birth in the Sonoran Desert, while the resident females remain and give birth in central Mexico. Using RAD-seq, we detected a demographic decline in this species during the Last Glacial Maximum and found that resident and migratory females form a single genetic cluster. Nevertheless, we identified 10 divergent genomic regions enriched with highly differentiated SNPs (FST values three or more orders of magnitude above the mean). Seven of such regions bear signatures of balancing selection and contain genes that have been identified in other migrating animals; such genes are qualitatively enriched for nervous system-related functions, potentially linked to circadian cycle, orientation, and navigation. Given that the migratory behavior is supposed to have originated recently in L. yerbabuenae (i.e., 10 to 20 Ka), we hypothesize that strong diversifying selection is operating in specific regions of the genome, while the rest is homogenized by the effect of males, which mate indistinctively with females from both groups.

Anthropized environments often fragment native habitats and alter the movement of individuals across the modified landscape mosaic, which is significantly challenging for wild species. Deciphering the environmental factors associated with population genetic patterns in modified habitats is essential to understand functional connectivity and for the conservation of wild populations inhabiting increasingly modified habitats. We used ddRAD-seq genomic data to study the genetic diversity, genetic structure and functional connectivity of the Giant Toad, Rhinella horribilis populations across two landscapes with distinct levels of habitat modification. We also applied a landscape genetics approach to identify landscape variables (climatic, vegetation, water bodies, land use) associated with the toad’s functional connectivity in both landscapes. Structure analysis between the two landscapes show that they are genetically differentiated given their distinct degree of habitat modification. Within landscapes, our results identified lower genetic diversity, higher genetic structure and lower functional connectivity among R. horribilis populations in the landscape with higher habitat modification. Results also demonstrate that structure and functional connectivity are significantly influenced by barriers like rivers and roads. Furthermore, water bodies availability was the most important landscape feature for R. horribilis connectivity, whereas vegetation cover, solar radiation and relative humidity also played a significant role. Our study illustrates how landscape features in modified habitats can differently determine genetic diversity and functional connectivity patterns, and highlights the importance of working with often-disregarded common species like the Giant Toad. Prioritizing the management of water bodies in our study sites and elsewhere would be essential to sustain amphibian population dynamics, enhancing individual movement and genetic exchange.

Local adaptation is a fundamental process that allows populations to thrive in their native environment, often increasing genetic differentiation with neighboring stands. However, detecting the molecular basis and selective factors responsible for local adaptation remains a challenge, particularly in sessile, non‐model species with long life cycles, such as forest trees. Local adaptation in trees is not only modeled by climatic factors, but also by soil variation. Such variation depends on dynamic geological and ecological processes that generate a highly heterogeneous selective mosaic that may differentially condition tree adaptation both at the range‐wide and local scales. This could be particularly manifest in species inhabiting mountain ranges that were formed by diverse geological events, like sacred fir ( Abies religiosa ), a conifer endemic to the mountains of central Mexico. Here, we used landscape genomics approaches to investigate how chemical edaphic variation influences the genetic structure of this species at the range‐wide and local scales. After controlling for neutral genetic structure, we performed genotype‐environment associations and identified 49 and 23 candidate SNPs at the range‐wide and local scales, respectively, with little overlap between scales. We then developed polygenic models with such candidates, which accounted for ~20% of the range‐wide variation in soil Ca ²⁺ concentration, electric conductivity ( EC ), and pH , and for the local variation in soil EC and organic carbon content ( OC ). Spatial Principal Component Analyses further highlighted the role of geography and population isolation in explaining this genetic‐soil co‐variation. Our findings reveal that local adaptation in trees is the result of an intricate interaction between soil chemical properties and the local population's genetic makeup, and that the selective factors driving such adaptation greatly vary and are not necessarily predictable across spatial scales. These results highlight the need to consider edaphic variation in forest genetic studies (including common garden experiments) and in conservation, management and assisted migration programs.

The presence of heterozygous individuals in a population is crucial for maintaining genetic diversity, which can positively affect fitness and adaptability to environmental changes. While inbreeding generally reduces the proportion of heterozygous individuals in a population, polyploidy tends to increase the proportion. North American Populus tremuloides is one of the most widely distributed and ecologically important tree species in the Northern Hemisphere. However, genetic variation in Mexican populations of P. tremuloides, including the genetic signatures of their adaptation to a variety of environments, remains largely uncharacterized. The aim of this study was to analyze how inbreeding coefficient (F_IS) and ploidy are associated with clonal richness, population cover, climate and soil traits in 91 marginal to small, isolated populations of this tree species throughout its entire distribution in Mexico. Genetic variables were determined using 36,810 filtered SNPs derived from genome re-sequencing. We found that F_IS was approximately between 0 and –1, indicating an extreme heterozygosity excess. One key contributor to the observed extreme heterozygosity excess was asexual reproduction, although ploidy levels cannot explain this excess. Analysis of all neutral SNPs showed that asexual reproduction was positively correlated with observed heterozygosity (H_o) but negatively correlated with expected heterozygosity (H_e). Analysis of outlier SNPs also showed that asexual reproduction was positively correlated with H_o and negatively correlated with H_e, although this latter correlation was not significant. These findings support the presence of a Meselson effect.

Anthropized environments are significantly challenging for wild species. Rapid adaptation to such habitats is thus key for their long-term persistence. Deciphering the environmental factors associated with species tolerance to modified habitats is fundamental for understanding the genetic and connectivity patterns of individuals and the local adaptation of their populations. We studied the Giant Toad, Rhinella horribilis, from two landscapes with distinct levels of anthropogenic habitat modification, assessed their genomic diversity, structure and connectivity with ddRAD-seq genomic data, identified potential outlier loci and their relationship with environmental and physicochemical water variables, and evaluated if populations from the two study sites showed signals of parallel adaptation. Both concordant and unique patterns were found regarding landscape factors and genotype-environment associations related with the degree of anthropic modification between landscapes. Genomic structure and connectivity were significantly associated with the presence of temporary water bodies, low vegetation cover, high humidity, solar radiation, and temperature. Notably, we identified both shared and distinct outlier SNPs and annotated functional genes for the two landscapes. Genes were enriched for biological processes and metabolic pathways, which were in turn correlated with environmental and physicochemical water variables. Genes and metabolic pathways were associated mainly with embryonic development, sexual maturation and immune responses. Studies such as this one, in an often-disregarded species, illustrate how parallel and un-parallel adaptive landscape genomic patterns arise in the stressful conditions of anthropized habitats.

Summary: Population genetics theory predicts a relationship between fitness, genetic diversity (H₀) and effective population size (N_e), which is often tested through heterozygosity‐fitness correlations (HFCs). We tested whether population and individual fertility and heterozygosity are correlated in two endangered Mexican spruces (Picea martinezii and Picea mexicana) by combining genomic, demographic and reproductive data (seed development and germination traits). For both species, there was a positive correlation between population size and seed development traits, but not germination rate. Individual genome‐wide heterozygosity and seed traits were only correlated in P. martinezii (general‐effects HFC), and none of the candidate single nucleotide polymorphisms (SNPs) associated with individual fertility showed heterozygote advantage in any species (no local‐effects HFC). We observed a single and recent (c. 30 thousand years ago (ka)) population decline for P. martinezii; the collapse of P. mexicana occurred in two phases separated by a long period of stability (c. 800 ka). Recruitment always contributed more to total population census than adult trees in P. mexicana, while this was only the case in the largest populations of P. martinezii. Equating fitness to either H₀ or N_e, as traditionally proposed in conservation biology, might not always be adequate, as species‐specific evolutionary factors can decouple the expected correlation between these parameters.

Air pollution caused by tropospheric ozone contributes to the decline of forest ecosystems; for instance, sacred fir,Abies religiosa(Kunth) Schltdl. & Cham. forests in the peri-urban region of Mexico City. Individual trees within these forests exhibit variation in their response to ozone exposure, including the severity of visible symptoms in needles. Using RNA-Seq metatranscriptomic data and ITS2 metabarcoding, we investigated whether symptom variation correlates with the taxonomic and functional composition of fungal mycobiomes from needles collected in this highly polluted area in the surroundings of Mexico City. Our findings indicate that ozone-related symptoms do not significantly correlate with changes in the taxonomic composition of fungal mycobiomes. However, genes coding for 30 putative proteins were differentially expressed in the mycobiome of asymptomatic needles, including eight genes previously associated with resistance to oxidative stress. These results suggest that fungal communities likely play a role in mitigating the oxidative burst caused by tropospheric ozone in sacred fir. Our study illustrates the feasibility of using RNA-Seq data, accessible from global sequence repositories, for the characterization of fungal communities associated with plant tissues, including their gene expression.

Urbanization modifies ecosystem conditions and evolutionary processes. This includes air pollution, mostly as tropospheric ozone (O₃), which contributes to the decline of urban and peri‐urban forests. A notable case are fir (Abies religiosa) forests in the peripheral mountains southwest of Mexico City, which have been severely affected by O₃ pollution since the 1970s. Interestingly, some young individuals exhibiting minimal O₃—related damage have been observed within a zone of significant O₃ exposure. Using this setting as a natural experiment, we compared asymptomatic and symptomatic individuals of similar age (≤15 years old; n = 10) using histologic, metabolomic, and transcriptomic approaches. Plants were sampled during days of high (170 ppb) and moderate (87 ppb) O₃ concentration. Given that there have been reforestation efforts in the region, with plants from different source populations, we first confirmed that all analyzed individuals clustered within the local genetic group when compared to a species‐wide panel (Admixture analysis with ~1.5K SNPs). We observed thicker epidermis and more collapsed cells in the palisade parenchyma of needles from symptomatic individuals than from their asymptomatic counterparts, with differences increasing with needle age. Furthermore, symptomatic individuals exhibited lower concentrations of various terpenes (ß‐pinene, ß‐caryophylene oxide, α‐caryophylene, and ß‐α‐cubebene) than asymptomatic trees, as evidenced through GC–MS. Finally, transcriptomic analyses revealed differential expression for 13 genes related to carbohydrate metabolism, plant defense, and gene regulation. Our results indicate a rapid and contrasting phenotypic response among trees, likely influenced by standing genetic variation and/or plastic mechanisms. They open the door to future evolutionary studies for understanding how O₃ tolerance develops in urban environments, and how this knowledge could contribute to forest restoration.