North African fox genomes show signatures of repeated introgression and adaptation to life in deserts

Rocha, Joana L.; Silva, Pedro M.; Santos, Nuno; Nakamura, Mónia; Afonso, Sandra; Qninba, Abdeljebbar; Boratyński, Zbyszek; Sudmant, Peter H.; Brito, José Carlos; Nielsen, Rasmus; Godinho, Raquel

doi:10.1038/s41559-023-02094-w

Cited by 15 publications

(7 citation statements)

References 127 publications

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“…Conversely, C. vipera is smaller, strictly hornless and specialized in burrowing in sandy substrates, with specific adaptations such as the dorsal position of the eyes (Young & Morain, 2003; Sivan et al, 2013). This morphological-genomic contrasting pattern has also been reported for other species with complex evolutionary histories present in desert environments as foxes (Leite et al, 2015; Rocha et al 2023).…”

Section: Discussionsupporting

confidence: 75%

“…2C). This discovery opens up avenues for future research to investigate the introgressed DNA regions and how this introgression could have affected the populations of C. c. cerastes compared to C. c. hoofieni , as introgression has been suggested as a source of adaptive variation (Hedrick, 2013) and has been proven fundamental for the arid adaption of some species of mammals (Liu et al, 2021; Nanaei et al 2023; Rocha et al 2023). Undoubtedly, additional individuals of C. vipera from northeastern Africa should be sampled to verify whether this introgression is maintained along the whole species’ range.…”

Section: Discussionmentioning

confidence: 99%

“…Remarkably, the advent of molecular genomics has allowed for the identification and characterization of introgression (i.e., the process by which genetic material from one species is incorporated into the genome of another species through interbreeding; Harrison & Larson, 2014) with increasing accuracy (Cahill et al, 2015; Leonard et al, 2013; Ottenburghs et al, 2017), confirming its significant impact on the evolution, adaptation and diversity of many species, including adaptive radiations (Seehausen, 2004). Adaptive introgression (the transfer of alleles from one species to another favored by natural selection) has even been proposed as another potential source of adaptation, aside from new mutations or standing variation (Hedrick, 2013), and has been reported to be involved in pesticide resistance, color polymorphism or adaptation to arid environments, among others (Anderson et al, 2009; Liu et al, 2021; Nanaei et al 2023; Rocha et al 2023; Song et al 2011).…”

Section: Introductionmentioning

confidence: 99%

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Hidden in the sand: phylogenomics unravel an unexpected evolutionary history on the desert-adapted vipers of the genusCerastes

Mochales-Riaño,

Burriel-Carranza,

Barros

et al. 2023

Preprint

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The desert vipers of the genusCerastesare a small clade of medically important venomous snakes within the family Viperidae. According to published morphological and molecular studies, the group is comprised by four species: two morphologically similar and phylogenetically sister taxa, the African horned viper (Cerastes cerastes) and the Arabian horned viper (Cerastes gasperettii); a more distantly related species, the Saharan sand viper (Cerastes vipera), and the enigmatic Böhme’s sand viper (Cerastes boehmei), only known from a single specimen in captivity allegedly captured in Central Tunisia. In this study, we analyzed one mitochondrial marker (COI) as well as genome-wide data (ddRAD sequencing) from 28 and 41 samples, respectively, covering the entire distribution range of the genus to explore the population genomics, phylogenomic relationships and introgression patterns within the genusCerastes. Additionally, and to provide insights into the mode of diversification of the group, we carried out niche overlap analyses considering climatic and habitat variables. Both nuclear phylogenomic reconstructions and population structure analyses have unveiled an unexpected evolutionary history for the genusCerastes, which sharply contradicts the morphological similarities and previously published mitochondrial approaches.Cerastes cerastesandC. viperaare recovered as sister taxa whilstC. gasperettiiis a sister taxon to the clade formed by these two species. We found a relatively high niche overlap (OI > 0.7) in both climatic and habitat variables betweenC. cerastesandC. vipera, contradicting a potential scenario of sympatric speciation. These results are in line with the introgression found between the northwestern African populations ofC. cerastesandC. vipera. Finally, our genomic data confirms the existence of a lineage ofC. cerastesin Arabia. All these results highlight the importance of genome-wide data over few genetic markers to study the evolutionary history of species.

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Section: Discussionsupporting

confidence: 75%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Hidden in the sand: phylogenomics unravel an unexpected evolutionary history on the desert-adapted vipers of the genusCerastes

Mochales-Riaño,

Burriel-Carranza,

Barros

et al. 2023

Preprint

Self Cite

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“…In Rueppell's fox, SLCO4A1, a solute carrier protein that can transport T4 is under positive selection, and a sulfotransferase implicated in TH metabolism showed a signature of selection. In accordance with these data, these two foxes displayed significantly lower levels of T4 than the African red fox (Vulpes vulpes) did [28]. It is very clear from all these cases that thermal regulation is intimately linked to metabolic activity.…”

Section: (B) Thermal Adaptationsupporting

confidence: 80%

The ecological function of thyroid hormones

Zwahlen,

Gairin,

Vianello

et al. 2024

Phil. Trans. R. Soc. B

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Thyroid hormones (TH) are central hormonal regulators, orchestrating gene expression and complex biological processes vital for growth and reproduction in variable environments by triggering specific developmental processes in response to external cues. TH serve distinct roles in different species: inducing metamorphosis in amphibians or teleost fishes, governing metabolic processes in mammals, and acting as effectors of seasonality. These multifaceted roles raise questions about the underlying mechanisms of TH action. Recent evidence suggests a shared ecological role of TH across vertebrates, potentially extending to a significant portion of bilaterian species. According to this model, TH ensure that ontogenetic transitions align with environmental conditions, particularly in terms of energy expenditure, helping animals to match their ontogenetic transition with available resources. This alignment spans post-embryonic developmental transitions common to all vertebrates and more subtle adjustments during seasonal changes. The underlying logic of TH function is to synchronize transitions with the environment. This review briefly outlines the fundamental mechanisms of thyroid signalling and shows various ways in which animals use this hormonal system in natural environments. Lastly, we propose a model linking TH signalling, environmental conditions, ontogenetic trajectory and metabolism. This article is part of the theme issue ‘Endocrine responses to environmental variation: conceptual approaches and recent developments’.

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“…This is particularly intriguing in the context of exploring adaptations to extreme conditions, given that the management of water has significant implications for survival. Studies have largely focused on characterizing the response in kidneys (Rocha et al, 2023;MacManes, 2017;Peng et al, 2023;Rocha et al, 2021), which, while important, represent only a fraction of the physiological and genomic response to dehydration. Indeed, the organismal response to an environmental stressor (such as dehydration), is likely to involve coordination of multiple organ systems and physiological process.…”

Section: Discussionmentioning

confidence: 99%

When the tap runs dry: The multi-tissue gene expression and physiological responses of water deprivedPeromyscus eremicus

Blumstein,

MacManes

2024

Preprint

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The harsh and dry conditions of desert environments have resulted in genomic adaptations, allowing for desert organisms to withstand prolonged drought, extreme temperatures, and limited food resources. Here, we present a comprehensive exploration of gene expression across five tissues (kidney, liver, lung, gastrointestinal tract, and hypothalamus) and 19 phenotypic measurements to explore the whole-organism physiological and genomic response to water deprivation in the desert-adapted cactus mouse (Peromyscus eremicus). The findings encompass the identification of differentially expressed genes and correlative analysis between phenotypes and gene expression patterns across multiple tissues. Specifically, we found robust activation of the vasopressin renin-angiotensin-aldosterone system (RAAS) pathways, whose primary function is to manage water and solute balance. Animals reduce food intake during water deprivation, and upregulation of PCK1 highlights the adaptive response to reduced oral intake via its actions aimed at maintained serum glucose levels. Even with such responses to maintain water balance, hemoconcentration still occurred, prompting a protective downregulation of genes responsible for the production of clotting factors while simultaneously enhancing angiogenesis which is thought to maintains tissue perfusion. In this study, we elucidate the complex mechanisms involved in water balance in the desert-adapted cactus mouse, P. eremicus. By prioritizing a comprehensive analysis of whole-organism physiology and multi-tissue gene expression in a simulated desert environment, we describe the complex and successful response of regulatory processes.

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North African fox genomes show signatures of repeated introgression and adaptation to life in deserts

Cited by 15 publications

References 127 publications

Hidden in the sand: phylogenomics unravel an unexpected evolutionary history on the desert-adapted vipers of the genusCerastes

Hidden in the sand: phylogenomics unravel an unexpected evolutionary history on the desert-adapted vipers of the genusCerastes

The ecological function of thyroid hormones

When the tap runs dry: The multi-tissue gene expression and physiological responses of water deprivedPeromyscus eremicus

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