How populations of aquatic fauna persist in extreme desert environments is an enigma. Individuals often breed and disperse during favourable conditions. However, theory predicts that adaptive capacity should be low in small populations, such as in desert fishes. We integrated satellite-derived surface water data, neutral population dynamics and adaptive evolution to understand metapopulation persistence across the range of the desert rainbowfish, central Australia. Desert rainbowfish showed very small population sizes, especially at peripheral populations, and low connectivity between river catchments. Yet, there was no evidence of population-level inbreeding and there was adaptive divergence associated with aridity. Candidate adaptive genes included functions related to environmental cues and stressful conditions. Evolutionary modelling showed that selection in refugial sub-populations combined with connectivity during flood periods can enable retention of adaptive diversity. Our study demonstrates that adaptive evolution can occur in small populations and integrate with neutral metapopulation processes to allow persistence in the desert.

Heterogeneous seascapes and strong environmental gradients in coastal waters are expected to influence adaptive divergence, particularly in species with large population sizes where selection is expected to be highly efficient. However, these influences might also extend to species characterized by strong social structure, natal philopatry and small home ranges. We implemented a seascape genomic study to test this hypothesis in Indo-Pacific bottlenose dolphins (Tursiops aduncus) distributed along the environmentally heterogeneous coast of southern Australia. The datasets included oceanographic and environmental variables thought to be good predictors of local adaptation in dolphins and 8,081 filtered single nucleotide polymorphisms (SNPs) genotyped for individuals sampled from six different bioregions. From a neutral perspective, population structure and connectivity of the dolphins were generally influenced by habitat type and social structuring. Genotype-environment association analysis identified 241 candidate adaptive loci and revealed that sea surface temperature and salinity gradients influenced adaptive divergence in these animals at both large- (1,000s km) and fine-scales (<100 km). Enrichment analysis and annotation of candidate genes revealed functions related to sodium-activated ion transport, kidney development, adipogenesis and thermogenesis. The findings of spatial adaptive divergence and inferences of putative physiological adaptations challenge previous suggestions that marine megafauna is most likely to be affected by environmental and climatic changes via indirect, trophic effects. Our work contributes to conservation management of coastal bottlenose dolphins subjected to anthropogenic disturbance and to efforts of clarifying how seascape heterogeneity influences adaptive diversity and evolution in small cetaceans.

Wildlife species are challenged and threatened by various infectious diseases that act as important selective forces and demographic drivers of populations. Yet, studies about host genetic factors and disease susceptibility are very limited. Cetacean morbillivirus (CeMV) has emerged as a major viral threat to cetacean populations worldwide, contributing to the death of tens of thousands of individuals of multiple dolphin and whale species. To understand the genomic basis of immune responses to CeMV, we generated and analysed whole genomes of 53 Indo-Pacific bottlenose dolphins (Tursiops aduncus) exposed to Australia’s largest CeMV-related mortality event known to date. The genomic dataset consisted of 7,720,686 SNPs anchored onto 23 chromosome-length scaffolds and 77 short scaffolds. Allele frequency estimates between survivors and non-survivors of the outbreak revealed 11,009 candidate SNPs, of which 498 were annotated to 220 protein coding genes. These included 36 genes with functions related to innate and adaptive immune responses, and cytokine signalling pathways. The list also included genes known to be involved in immune responses to other morbilliviruses, such as measles in humans and the phocine distemper virus in pinnipeds. Our study characterised genomic regions and pathways that likely contribute to CeMV susceptibility and resistance in dolphins, representing a stride towards clarifying the complex interactions of the cetacean immune system. It also emphasises the relevance of whole genome datasets to study the genetics of wildlife diseases.