The geno-geo-climate nexus: contributions of geographic and ecological factors in shaping the genomic divergence of two closely related threatened rainforest species of Fontainea Heckel (Euphorbiaceae)

Abstract

Context: Processes that shape genomic and ecological divergence can reveal important evolutionary dynamics to inform the conservation of threatened species. Fontainea is a genus of rainforest shrubs and small trees including critically endangered and threatened species restricted to narrow, but complex geographic and ecological regions. Several species of Fontainea are subject to spatially explicit conditions and experience limited intra-specific gene flow, likely generating genetic differentiation and local adaptation. Objectives: Here, we explored the genetic and ecological mechanisms underlying patterns of diversification in two, closely related threatened Fontainea species. Our aim was to compare spatial patterns of genetic variation between the vulnerable Fontainea australis (Southern Fontainea) and critically endangered F. oraria (Coastal Fontainea), endemic to the heterogeneous subtropical region of central, eastern Australia, where large-scale clearing has severely reduced rainforest habitat to a fraction (< 1%) of its pre-European settlement extent. Methods: We used a set of 10,000 reduced-representation markers to infer genetic relationships and the drivers of spatial genetic variation across the two species. In addition, we employed a combination of univariate and multivariate genome-environment association analysis using a set of topo-climatic variables to explore potential patterns of local adaptation as a factor impacting genomic divergence. Results: Our study revealed that Coastal Fontainea have a close genetic relationship with Southern Fontainea. We showed that isolation by distance has played a key role in their genetic variation, indicating that vicariance can explain the spatial genetic distribution of the two species. Genotype-environment analyses showed a strong association with temperature and topographic features, suggesting adaptation to localised thermal environments. We used a multivariate redundancy analysis to identify a range of putatively adapted loci associated with local environmental conditions. Conclusions: Divergent selection at the local-habitat scale as a result of dispersal limitations and environmental heterogeneity (including physical barriers) are likely contributors to adaptive divergence between the two Fontainea species. Our findings have presented evidence to indicate that Southern and Coastal Fontainea were comprised of distinct genetic groups and ecotypes, that together may form a single species continuum, with further phenotype research suggested to confirm the current species boundaries. Proactive conservation actions, including assisted migration to enhance the resilience of populations lacking stress-tolerant single nucleotide polymorphisms (SNPs) may be required to secure the long-term future of both taxa. This is especially vital for the critically endangered Coastal Fontainea given projections of habitat decline for the species under future climate scenarios.