Fish out of water: Genomic insights into persistence of rainbowfish populations in the desert

Abstract

How populations of aquatic fauna persist in extreme desert environments is an enigma. Individuals often breed and disperse during favorable conditions. Theory predicts that adaptive capacity should be low in small populations, such as in desert fishes. We integrated satellite-derived surface water data and population genomic diversity from 20,294 single-nucleotide polymorphisms across 344 individuals to understand metapopulation persistence of the desert rainbowfish (Melanotaenia splendida tatei) in central Australia. Desert rainbowfish showed very small effective population sizes, especially at peripheral populations, and low connectivity between river catchments. Yet, there was no evidence of population-level inbreeding and a signal of possible adaptive divergence associated with aridity was detected. Candidate genes for local adaptation included functions related to environmental cues and stressful conditions. Eco-evolutionary modeling showed that positive selection in refugial subpopulations combined with connectivity during flood periods can enable retention of adaptive diversity. Our study suggests that adaptive variation can be maintained in small populations and integrate with neutral metapopulation processes to allow persistence in the desert.

Aridification‐driven evolution of a migratory fish revealed by niche modelling and coalescence simulations

“…Nevertheless, approaches that incorporate data from regional climate models (e.g. Attard, Sandoval-Castillo, Brauer, et al, 2022;Buckley et al, 2021) can produce reasonable hypotheses to be tested through a coalescent framework at a basin and lineage level, as demonstrated here.…”

“…Freshwater ecosystems are severely threatened on a global scale due a multitude of factors such as habitat degradation, pollution and water extraction (Williams‐Subiza & Epele, 2021). In arid settings, these stresses are exacerbated by the natural isolation of water bodies (Attard, Sandoval‐Castillo, Brauer, et al, 2022; Murphy et al, 2015). The Australian arid zone contains various types of freshwater habitats, ranging from ephemeral rivers and isolated waterholes to permanent groundwater‐fed springs (Fensham et al, 2011).…”

“…The Australian arid zone contains various types of freshwater habitats, ranging from ephemeral rivers and isolated waterholes to permanent groundwater‐fed springs (Fensham et al, 2011). These systems are often connected during high rainfall events, facilitating organismal dispersal between localities (Attard, Sandoval‐Castillo, Brauer, et al, 2022; Fensham et al, 2011). Anthropogenic climate change is projected to increase aridity over much of Australia in coming decades, leading to more variable flow regimes and declines in water connectivity (Larkin et al, 2020).…”

Weaving place‐based knowledge for culturally significant species in the age of genomics: Looking to the past to navigate the future

“…Genetic and genomic studies have long recognized how complex evolutionary dynamics, such as gene flow, shape genetic diversity, including local adaptation (e.g., Attard et al, 2021; Beheregaray & Caccone, 2007; Ralls et al, 2018; Tigano & Friesen, 2016). For culturally significant species, these dynamics are often linked to IPLC knowledge and practices.…”

Riverscape Genomics Clarifies Neutral and Adaptive Evolution in an Amazonian Characin Fish (Triportheus albus)

“…Limited research has explained how natural selection acts in aquatic environments (Kelley et al, 2016;Grummer et al, 2019). In rivers and streams, a constrained, unidirectional spatial flow of genes along well-defined migratory paths provides an ideal environment for the study of natural selection, as the impacts of geographic separation on genetic divergence can be controlled for (Hughes et al, 2009;Brauer et al, 2018;Attard et al, 2022). The Amazon, also known as Amazonia, holds the highest diversity of freshwater fishes in the world, yet little is understood about their evolution (Corlett and Primack, 2010;Beheregaray et al, 2014).…”