Landscape genomics and adaptive resilience to climate change of the tropical rainbowfish (Melanotaenia splendida splendida)

Author: Katie Gates

  • Thesis download: available for open access on 18 Mar 2025.

Gates, Katie, 2022 Landscape genomics and adaptive resilience to climate change of the tropical rainbowfish (Melanotaenia splendida splendida), Flinders University, College of Science and Engineering

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As ecosystems are exposed to rapidly changing climates, impacts may depend not only on magnitudes of change, but on organisms’ existing physiologies, plastic capacities, and their potential for evolutionary adaptation. These factors are likely to vary among environments, and in accordance with local or regional biogeographic influences. Tropical regions, and particularly freshwater environments, remain understudied relative to their temperate counterparts, and disputes exist about evolutionary mechanisms in these hyper-diverse landscapes. We therefore aimed to clarify how hydroclimatic selection and landscape structure shape intraspecies adaptive diversity and evolution of an Australian tropical-endemic rainbowfish, Melanotaenia splendida splendida, as well as resilience under rapid climatic change.

Our first two data chapters employed a comparative riverscape-based approach, integrating genomic, phenotypic, and environmental datasets (14,540 filtered SNPs, 18 morphometric landmarks, and eight hydrological attributes, respectively) for 381 individuals from 17 sampling sites across rainforest and savannah biomes. Environmental associations both within and among these contrasting and heterogeneous habitats allowed us to test contributions of adaptive and non-adaptive influences on intraspecies diversity. Strong ecotype-specific environmental associations provided evidence for divergent adaptations to hydroclimate. Moreover, environment was a better predictor of genetic and morphological variation than neutral or spatial factors. This was particularly evident for body shape, which was relatively poorly explained by neutral population structure. Given that similar trait divergence has been associated with heritable hydrodynamic-related variation in congeneric species, this may reflect important functional consequences of body shape variation. Additional combined associations between genotype, phenotype, and environment supported the tentative inference of evolved adaptive differences. Weaker adaptive signals in the more connected savannah ecotype were consistent with a homogenising effect of gene flow on local adaptation.

In our third data chapter, we used experiments to compare short-term responses to climate warming among rainforest and savannah ecotypes, as well as in relation to previously studied temperate, desert, and subtropical rainbowfish ecotypes. Specifically, we assessed rapid acclimation capacity via tests of critical thermal maxima, as well as transcriptional responses to projected 2070 summer temperatures using differential expression analysis. We identified 189 DE genes as candidates for future thermal responses, including hub genes related to heat shock and lipid metabolism. We found a strong positive relationship between induced transcriptional responses and upper thermal tolerance, both of which were greater in the savannah ecotype. Meanwhile, the rainforest ecotype’s more limited plastic capacity may reflect greater specialisation of thermal responses suited to its more temporally stable native environment.

Our work suggests that both contemporary hydroclimatic variation and drainage connectivity have shaped regional diversity in this species, with possible trade-offs between system-wide and locally specialised adaptations among rainforest and savannah ecotypes. We expect that alteration of current climates will necessitate substantial evolutionary responses for in situ population persistence, and that these may be more constrained in the climatically stable rainforest biome. Overall, the findings contribute to broader discussions about mechanisms promoting and maintaining patterns of tropical diversity, and highlight the utility of integrating diverse biological datasets to better disentangle complex evolutionary processes.

Keywords: Australia, climate change, comparative genomics, comparative transcriptomics, ddRAD-seq, ecological adaptation, freshwater fish, gene flow, genotype-phenotype-environment, morphometrics, population divergence, rainbowfish, rainforest, RNA-seq, savannah, thermal tolerance, tropical diversity

Subject: Biological Sciences thesis

Thesis type: Doctor of Philosophy
Completed: 2022
School: College of Science and Engineering
Supervisor: Luciano Beheregaray