Life in Deserts: The Genetic Basis of Mammalian Desert Adaptation

Abstract

Deserts are among the harshest environments on Earth. The multiple ages of different deserts and their global distribution provide a unique opportunity to study repeated adaptation at different timescales. Here, we summarize recent genomic research on the genetic mechanisms underlying desert adaptations in mammals. Several studies on different desert mammals show large overlap in functional classes of genes and pathways, consistent with the complexity and variety of phenotypes associated with desert adaptation to water and food scarcity and extreme temperatures. However, studies of desert adaptation are also challenged by a lack of accurate genotype-phenotype-environment maps. We encourage development of systems that facilitate functional analyses, but also acknowledge the need for more studies on a wider variety of desert mammals.

Keywords: adaptation; desert; genomics; mammals; physiology.

Figure 1.. Genomic Approaches Used to Identify Genes Underlying Desert Adaptation.

(A) Population-based methods, (B) comparative-based methods, and (C) differential expression analyses in natural (i) and laboratory (ii) conditions. (A–C) Different silhouettes represent distinct species, silhouettes in orange represent desert populations/species, and gray silhouettes represent non-desert populations/species under comparison and outgroups; double-headed arrows represent the comparison being made, one-headed arrows represent the group or lineage targeted by the method; ‘X’ represents a condition of experimental dehydration or water deprivation, as opposed to animals being given water. (D) Schematic representation synthesizing and relating some of the recently discovered genes and functional gene classes to previously described phenotypes. Functional connections result from gene ontology enrichment analyses of sets of candidate genes and/or gene-function annotation (Gene Cards, OMIM, and UniProt). Some of the highlighted genes identified with population-based and comparative-based methods on whole genomes and DNA sequences of candidate genes found differentially expressed are represented with superscripts as follows: En – Endurers (1, Bactrian camel, Camelus bactrianus; 2, Dromedary camel, Camelus dromedarius; 3, Taklamakan and 4, Barki sheep, Ovis aries; 5, Barki goat, Capra hircus; 6, arid-dwelling Asian sheep); Ev – Evaders (1, Cactus mouse, Peromyscus eremicus; 2, Canyon mouse Peromyscus citrinus; 3, House mouse, Mus musculus; 4, Patagonian olive mouse, Abrothrix olivacea; 5, Banner-tailed kangaroo rat, Dipodomys spectabilis; 6, Bailey’s pocket mouse, Chaetodipus baileyi); H – humans (Aboriginal Australians).

Figure 2.. Shared Evidence of Selection in Genes (A) and Gene Ontology (GO) Terms and Pathways (B) Obtained from Comparative and Population Genomics in Evader (Ev), Endurer (En), and Human (H) Case Studies.

Examples reviewed here include: Cactus mouse (Peromyscus eremicus) [18], Canyon mouse (Peromyscus citrinus) [21], Tarim red deer (Cervus elaphus yarkandensis) [16], arid-dwelling Asian and Taklamakan desert sheep (Ovis aries) [13], Bactrian camel (Camelus bactrianus) [32,34], Dromedary camel (Camelus dromedarius) [32], North-African Barki sheep (O. aries) and goat (Capra hircus) [17], Nubian Ibex (Capra nubiana) [39], and southern African Khoe-San [57] and Aboriginal Australians [12] (Homo sapiens). The significance of gene and GO overlap was calculated using Fisher’s exact test on a contingency table. Significant overlap is represented by colors standing out against the lightest background (marginal P values >0.05).

Figure I.. The Different Steps for Future Research Attempting to Integrate Available Methodologies to Address the Genomic Basis of Desert Adaptation.

(A) Simultaneous collection of genomic, transcriptomic (across different tissues and also blood), phenotypic (see Box 1 in the main text), and climatic data (e.g., WorldClim database). Data collection under common garden and field reciprocal transplant experiments is suggested for model organisms (e.g., Mus and Peromyscus spp.). For common garden experiments, we suggest different combinations of environmental stressors. Different silhouettes represent distinct species, silhouettes in orange represent desert populations/species, and gray silhouettes represent non-desert populations/species; double-headed arrows represent the comparison being made; ‘X’ represents a condition of experimental dehydration or water deprivation, as opposed to animals being given water. (B) Diverse ways in which different data sets can be combined for methods in population and comparative genomics, depending on data availability and the evolutionary context of the study system of choice. The strength of selection studies is that they are powerful for identifying candidates for further testing. (C) Experimental validation of candidate genes under selection (CRISPR-Cas 9 and cell culture).