A genomic perspective on adaptation to heterogeneous environments for Cycas segmentifida (Cycadaceae), an endemic cycad in southwest China

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Abstract Background and Aims Exploring the interplay of environmental variability and adaptation of an endemic species is essential to unravel its evolutionary history and lays the groundwork for assessing how it may react to the accelerating pace of climate change. Employing a population genomics method, this research sought to investigate the adaptation of a cycad species, Cycas segmentifida, to heterogeneous environments and how this fosters population differentiation, guiding its conservation efforts. Methods We used double digest restriction-site associated DNA-sequencing (ddRAD-seq) to elucidate the pattern of genetic diversity and divergence, and then analyze how geographical and environmental factors contribute to population divergence in C. segmentifida. We further investigate the genetic basis of adaptation to heterogeneous environments and their implications for predicting its genomic vulnerability under future climate conditions. Key Results Cycas segmentifida can be geographically categorized into two genetic groups: the Northwest (NW) and the Southeast (SE) group, with the genetic diversity of the SE group significantly higher than the NW group. Both geographical distance and environment factors could explain this genetic structure. These two groups exhibited similar demographic histories from late Pliocene to middle Pleistocene, experiencing recent population contraction events. The Genotype-environment association analysis revealed significant differences in environmental variables between two habitats of C. segmentifida, suggesting the possible existence of adaptation. The genomic vulnerability of C. segmentifida is relatively low throughout its distribution range, suggesting its potential to cope with future climate changes. Conclusions Our results unveil environmental heterogeneity profoundly influences the genetic structure of C. segmentifida, and provide understanding of its sensitivity to climate change and capacity for adaptive responses, guiding future conservation endeavors.