Exposure of mammal genetic diversity to mid-21st century global change

By Spyros Theodoridis

Climate and land-use change are accelerating and taking their toll on all aspects of biodiversity, from genes, to species, to ecosystems. In response to this crisis, the vast majority of conservation efforts has so far focused on protecting biodiversity at the species and/or ecosystem levels, while the revisited post-2020 goals of the Convention on Biological Diversity (CBD) are still overlooking genetic diversity in natural populations (Laikre et al. 2020). Genetic diversity is a — if not the most — fundamental element of biodiversity, playing a major role in life’s capacity to adapt to changing environments, thus maintaining healthy ecosystems and the goods they provide to humanity. Yet, the lack of global scale genetic data for wild populations has hindered any assessments on the threats that global environmental change imposes on genetic diversity. The ultimate goal of our study was to produce the first global map of the exposure of mammal genetic diversity to mid-21st century climate and land-use change, hopefully contributing towards the prioritization of this important aspect of biodiversity conservation.

Ever since I started doing research, I was fascinated with the fact that a single molecule (i.e. DNA) has the ability to act both as a "storyteller" and as a "prophet". Genetic diversity can act as a "storyteller" because it stores and reflects all the changes that have happened throughout a species lifetime, i.e. its origination time, its migration routes, its establishment to new territories, and its demographic fluctuations in response to its environment. It can also act as a "prophet" because it provides insights whether a species will go extinct or thrive in response to future environmental change. This is particularly relevant for the potential effects of global warming on biodiversity, where a growing body of research highlights the dual role of variation, even the so-called “neutral”, in the mitochondrial genome both in reflecting local adaptation to climate and in determining the thermal range that an organism can tolerate. High levels of mitochondrial genetic diversity, particularly in warmer climates, could provide heat tolerance and buffer against rapid warming, while low levels may render species incapable of responding to rising temperatures. This realization makes the need to assess the global distribution of genetic diversity and its exposure under global change even more pressing.

Figure 1 Predicted intraspecific genetic diversity in mammal assemblages for two mitochondrial genes, cytb and co1. (grid-cells at 385.9 × 385.9 km spatial resolution).

Driven by this need, a few years ago David Nogués-Bravo and his team started fetching mitochondrial sequences deposited in public repositories and attaching geographic coordinates to them. This exercise resulted in the first-ever map of genetic diversity in wild animal populations (Miraldo et al. 2016). But these maps were still incomplete with lots of gaps, particularly in biodiversity-rich regions, such as the tropics. The team continued to compile data and a couple of years later we joined forces to take the next step. The enriched data set enabled the identification of global covariates of mammal mitochondrial genetic diversity, including phylogenetic diversity and past climate change (Theodoridis et al. 2020). These correlates allowed us to model and predict the distribution of genetic diversity globally and obtain complete maps (Fig. 1) where we could overlay novel climate and land-use change scenarios for the 21st century. Although we were all very fascinated with these advancements, our results are rather alarming.

We found that more than 50% of the genetically poorest geographic areas (grid-cells), primarily distributed in tundra, boreal forests/taiga and temperate bioclimatic regions, will be exposed to mean annual temperature rise that exceeds 2°C compared to the baseline period under all considered future scenarios (Fig. 2). We also showed that at least 30% of the most genetically rich areas in tropical, subtropical and montane regions will be exposed to an increase of mean annual temperature > 2°C under less optimal scenarios. There are two key messages in these results. Species and populations at higher latitudes are facing severe exposure to rising temperatures and given their low genetic diversity may not be able to adapt. On the other hand, species in the tropics contain high levels of genetic diversity, potentially providing them with an adaptation shield to global warming, but will have to face the direct human pressure, such as deforestation and overexploitation.

Figure 2 Exposure of mammal cytb genetic diversity to climate and land-use change across three future scenarios (SSPs). In the color scales, the x-axis indicates genetic diversity split in quartiles. The y-axis indicates the change (i.e. exposure) between future and baseline values for each climate and land-use variable.

The relevance of our assessment for the future of life on our planet has already attracted the attention of international instruments, such as the Secretariat of the United Nations Convention on Biological Diversity for informing their conservation strategies and agendas. It has also been distributed from human health related outlets (Hinsley 2021) indicating the importance of protecting genetic diversity in the wild for maintaining healthy human societies. We hope that these results will pave the road to better estimate the geography of biodiversity vulnerability to global change and collectively act before it's too late.

References

Hinsley S. 2021. Planetary Health Research Digest. Lancet Planet. Health 5: e190.

Laikre L. et al. 2020. Post-2020 goals overlook genetic diversity. –  Science 367 1083-1085.

Miraldo A. et al. 2016. An Anthropocene map of genetic diversity. – Science 353: 1532–1535.

Theodoridis S. et al. 2020. Evolutionary history and past climate change shape the distribution of genetic diversity in terrestrial mammals. – Nat. Comm.11: 2557.

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