Which genes and functions respond to environmental change?

This blog post is provided by Katharina Wollenberg Valero and tells the #StoryBehindThePaper for the paper “Functional genomics of abiotic environmental adaptation in lacertid lizards and other vertebrates“, which was recently published in the Journal of Animal Ecology. This paper is part of the Journal of Animal Ecology Special Feature: “Understanding climate change response in the age of genomics”. In their study, they investigate which genes and functions determine adaptation to the abiotic environment and whether distinct species use similar or different genes for this

Our rapidly changing climate, both in terms of slowly increasing global temperature and in terms of weather extremes, requires us to better understand the genetic mechanisms by which animals respond to changes in their abiotic environment. Comparing the genomes of different species which have adapted to very diverse environmental conditions in the past with each other, could enable us to distinguish which of the approximately ~20,000 genes in a genome are used to adapt to environmental changes, and which functions these genes have. In our study, we compared the widespread group of lacertid lizards with other vertebrates (Wollenberg Valero et al., 2021).

Podarcis muralis, a lacertid lizard. Photo credit: Miguel Vences.

Lacertid lizards occur in a wide variety of climates from the African Namib to the Arctic Circle, and from lowlands to mountainous regions. In a previous study (Garcia-Porta et al., 2019), we found that these lizards prefer temperatures that are closely aligned to the climate of the environment they inhabit, hinting at preferred temperatures being the result of genetic adaptation. In this present study, we used the same data set to identify these genes in lacertids and determine which of them align with changes in climate. We then compared these genes to those identified in other studies of vertebrates to gain a more comprehensive picture of which genes and functions determine adaptation to the abiotic environment, and whether distinct species use similar or different genes for this.

We first identified 200 genes under positive diversifying selection from our lacertid dataset (the true number may be higher as we only analyzed adult transcriptomes), with species living in hot areas having more genes under intensified selection than species living in cold areas. Several of these genes had experienced accelerated evolutionary rates in response to hot, warm, or cold climates (measured as average annual hours above 30℃ in each species’ habitat). There was also a (non-significant) trend for association of evolutionary rates of these genes between warm habitats and high preferred temperatures. In contrast, there was strong association of evolutionary rates of genes under selection of higher evaporative water loss (Figure 1) and general skeletal morphology with cooler habitats. This matches recent observations that water balance is an important physiological property determining resilience to climate change in squamate reptiles (Le Gaillard et al., 2021).

Figure 1. Negative correlation of evolutionary rate parameters between evaporative water loss (iwl) and hours above ℃ in 200 genes under positive diversifying selection in lacertid lizards.

We then compiled these genes into a dataset containing 902 genes under selection to different abiotic environments in other vertebrate species, from fish to humans. Functions of these genes matched up well (23%) with functions we previously predicted would be important for climate adaptation, based on a set of physiological responses commonly observed in response to changes in temperature (Wollenberg Valero et al., 2014; Rodriguez et al., 2017). However, “localization and transport” was also a new, unpredicted cellular function of many of these genes (Figure 2). Interestingly, these genes were strongly connected to each other functionally and were to 18% involved in the organismal stress response. It makes sense that adaptation to different environments involves alterations to stress response pathways.

Figure 2. Pie chart showing functions of 902 genes with signatures of selection to abiotic environmental changes. Cf denotes previously predicted candidate functions.

Another exciting discovery was that 43% of these genes responded to environment-related selection in more than one species. We tested whether this pattern was uncovered by chance, (just by means of accumulating genes from different studies), by running 100,000 simulations of the number of draws that need to be performed to find the same number of genes at least twice (from a reduced set of genes that have the same functions). This revealed that this number was unlikely to have happened by chance, and consequently our findings indicate that even in a pool of tens of thousands of genes, the fact that these genes are organized into functional modules may narrow down the evolutionary search space for beneficial variants in response to changing environments (see also Wollenberg Valero, 2020). Studies are already underway to identify or manipulate heat-resistant variants (e.g., in corals, Cleves et al., 2020). The identification of genes and functions causally involved with climate adaptation will further enable such work in the future.

Read the paper

Read the full paper here: Wollenberg Valero, K. C., Garcia-Porta, J., Irisarri, I., Feugere, L., Bates, A., Kirchhof, S., Jovanović Glavaš, O., Pafilis, P., Samuel, S. F., Müller, J., Vences, M., Turner, A. P., Beltran-Alvarez, P., & Storey, K. B. (2022). Functional genomics of abiotic environmental adaptation in lacertid lizards and other vertebrates. Journal of Animal Ecology, 91, 1163– 1179. https://doi.org/10.1111/1365-2656.13617

References
  • Cleves, P.A., Tinoco, A.I., Bradford, J., Perrin, D., Bay, L.K. and Pringle, J.R., 2020. Reduced thermal tolerance in a coral carrying CRISPR-induced mutations in the gene for a heat-shock transcription factor. Proceedings of the National Academy of Sciences, 117(46), pp.28899-28905
  • Garcia-Porta et al. Environmental temperatures shape thermal physiology as well as diversification and genome-wide substitution rates in lizards. Nature Communications 10:4077 (2019). Read online at: https://rdcu.be/bQE2n
  • Wollenberg Valero, K.C., Pathak, R., Prajapati, I., Bankston, S., Thompson, A., Usher, J. and Isokpehi, R.D., 2014. A candidate multimodal functional genetic network for thermal adaptation. PeerJ, 2, p.e578.
  • Rodríguez, A., Rusciano, T., Hamilton, R., Holmes, L., Jordan, D. and Wollenberg Valero, K.C., 2017. Genomic and phenotypic signatures of climate adaptation in an Anolis lizard. Ecology and evolution, 7(16), pp.6390-6403.
  • Wollenberg Valero, K.C., Garcia‐Porta, J., Irisarri, I., Feugere, L., Bates, A., Kirchhof, S., Jovanović Glavaš, O., Pafilis, P., Samuel, S.F., Müller, J. and Vences, M., 2021. Functional genomics of abiotic environmental adaptation in lacertid lizards and other vertebrates. Journal of Animal Ecology. https://doi.org/10.1111/1365-2656.13617
  • Wollenberg Valero, K.C., 2020. Aligning functional network constraint to evolutionary outcomes. BMC Evolutionary Biology, 20(1), pp.1-14.
  • Le Galliard, J.F., Chabaud, C., de Andrade, D.O.V., Brischoux, F., Carretero, M.A., Dupoué, A., Gavira, R.S., Lourdais, O., Sannolo, M. and Van Dooren, T.J., 2021. A worldwide and annotated database of evaporative water loss rates in squamate reptiles. Global Ecology and Biogeography, 30(10), pp.1938-1950.

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