The interplay among space, environment, and gene flow drives genetic differentiation in endemic Baja California Agave sobria subspecies.

Premise: Research on neutral and adaptive processes that lead to the divergence of species and populations is a crucial component in evolutionary and conservation genetics. Agave sobria is an endemic group of subspecies scattered on canyons along a latitudinal gradient and distinct environments of the Baja California Peninsula, Mexico. Agave sobria represents a unique opportunity to study the process of genetic differentiation in a highly heterogeneous environment.

Methods: Using genotyping-by-sequencing, we genotyped 8453 single-nucleotide polymorphisms (SNPs) in all A. sobria subspecies, including 19 A. sobria and three closely related A. cerulata ssp. subcerulata populations. We assessed neutral genetic structure and diversity at both the interspecific and intraspecific levels, evaluated the amount and direction of gene flow, and identified putatively adaptive SNPs.

Results: We found low support for the currently recognized subspecies. We detected neutral (i.e., isolation by distance) and adaptive divergence linked to eco-geographic characteristics of the habitat. High genetic connectivity indicated that gene flow between central and northern populations may have homogenizing effects preventing population differentiation. For the southernmost A. sobria ssp. frailensis, temperature and geographic isolation appear to be the main drivers of adaptive differentiation, with outlier SNPs located in coding regions involved in response to abiotic stress and immunology.

Conclusions: In A. sobria, environmental isolation and geographic gradients affect the genetic structure, creating opportunities for local adaptation. Our results emphasize the importance of including neutral and adaptive perspectives, the combination of which allows a better understanding of the complexity of the processes that lead to population differentiation.