Gene abundance linked to climate zone: Parallel evolution of gene content along elevation gradients in lichenized fungi

Abstract

IntroductionIntraspecific genomic variability affects a species’ adaptive potential toward climatic conditions. Variation in gene content across populations and environments may point at genomic adaptations to specific environments. The lichen symbiosis, a stable association of fungal and photobiont partners, offers an excellent system to study environmentally driven gene content variation. Many of these species have remarkable environmental tolerances, and often form populations across different climate zones. Here, we combine comparative and population genomics to assess the presence and absence of genes in high and low elevation genomes of two lichenized fungi of the genus Umbilicaria.MethodsThe two species have non-overlapping ranges, but occupy similar climatic niches in North America (U. phaea) and Europe (U. pustulata): high elevation populations are located in the cold temperate zone and low elevation populations in the Mediterranean zone. We assessed gene content variation along replicated elevation gradients in each of the two species, based on a total of 2050 individuals across 26 populations. Specifically, we assessed shared orthologs across species within the same climate zone, and tracked, which genes increase or decrease in abundance within populations along elevation.ResultsIn total, we found 16 orthogroups with shared orthologous genes in genomes at low elevation and 13 at high elevation. Coverage analysis revealed one ortholog that is exclusive to genomes at low elevation. Conserved domain search revealed domains common to the protein kinase superfamily. We traced the discovered ortholog in populations along five replicated elevation gradients on both continents and found that the number of this protein kinase gene linearly declined in abundance with increasing elevation, and was absent in the highest populations.DiscussionWe consider the parallel loss of an ortholog in two species and in two geographic settings a rare find, and a step forward in understanding the genomic underpinnings of climatic tolerances in lichenized fungi. In addition, the tracking of gene content variation provides a widely applicable framework for retrieving biogeographical determinants of gene presence/absence patterns. Our work provides insights into gene content variation of lichenized fungi in relation to climatic gradients, suggesting a new research direction with implications for understanding evolutionary trajectories of complex symbioses in relation to climatic change.

Circadian clock‐ and temperature‐associated genes contribute to overall genomic differentiation along elevation in lichenized fungi

“…Despite this difference in reproductive strategies, adaptation to different niches along elevation gradients may be linked to similar processes in both species, as evidenced by the presence or absence of particular enzymes in either climate zone (Merges et al, 2023). Adaptive responses of the circadian system to climate gradients are presently unknown in lichens.…”

Circadian clock and temperature-associated genes vary along climate gradients in lichenized fungi

“…Part of the observed population differentiation can be linked to environmental factors, evidenced, e.g., by abrupt, parallel genomic breaks along elevation gradients, separating populations into high and low elevation genetic clusters, which correspond to different climate zones (Dal Grande et al, 2017, Rolshausen et al, 2020, 2022. Adaptation to different niches along elevation gradients is likely linked to a variety of processes, including the potential to synthesize natural products (Singh et al 2021), or particular enzymes (Merges et al 2023), and evolution through mobile elements (Dal Grande et al 2021). Adaptive responses of the circadian system to climate gradients are presently unknown in lichens.…”