Katrina McGuigan

The phenotypic effects of mutations often depend on the genetic background, yet general patterns remain poorly resolved. Here, we tested whether same-population individuals (genotypes) with different breeding values for a polygenic trait differed in their contribution of new mutational variation to that trait. We analysed more than 44 000 wing-size measurements over 30 generations of mutation-drift evolution in four Drosophila serrata genotypes to quantify genotype-specific mutational variance and mutational bias for size. The smallest and largest breeding value genotypes contributed similar mutational variance. By contrast, the genotype associated with average size contributed effectively no mutational variance, had reduced micro-environmental variance, and high line survival, consistent with no mutational decay in fitness. Genotypes with detectable mutational input exhibited declines in mean size over time, indicating a consistent mutational bias towards smaller size. This bias appeared genotype dependent, nearly half as strong in the genotypes associated with smallest size. Together, these results demonstrate substantial heterogeneity in mutational properties among genotypes within a single natural population where the trait value spans a relatively narrow range. Such genotype-specific mutational input is expected to shape both the standing genetic variance and the evolutionary trajectory of polygenic traits.

Extreme climatic events are reshaping ecosystems worldwide as individual organisms vary markedly in their ability to withstand these disturbances. Deciphering patterns of persistence on local scales is therefore critical for predicting biodiversity trajectories under intensifying climate extremes. In this study, we examined variation in thermal stress responses among individuals of the coral Stylophora pistillata species complex during a heatwave at Heron Island Reef, Australia. More than half of the focal coral colonies died on the reef, and survival of coral fragments maintained under ex situ common thermal stress conditions was significantly correlated with the survival of their source colony. This demonstrates that survival differences result largely from biological factors rather than differential thermal exposure across reef habitats. Under common garden conditions, we observed striking differences in bleaching severity and survival times among three sympatric cryptic taxa and their highly host-specific symbiont community. Within the most locally common taxon, corals from historically warmer and more seasonally variable reef habitats seem more susceptible to bleaching, contrary to expectations. Together, these results reveal how biological differences among cryptic taxa and among individuals can shape coral responses during a heatwave and advance our understanding of coral vulnerability in a rapidly warming world.

The phenotypic effects of mutations often depend on the genetic background, yet general patterns remain poorly resolved. Here, we tested whether genotypes drawn from the same natural population, but differing in their breeding values for a polygenic trait, differed in their contribution of new mutational variation to that trait. We established >200 mutation-accumulation (MA) lines from four Drosophila serrata genotypes. Analysing >44,000 wing-size measurements, collected over 30 generations, we quantified mutational variance and mutational bias for size. Genotypes with the smallest and largest breeding values for size contributed similar (statistically indistinguishable) amounts of mutational variance. In contrast, the genotype with an intermediate breeding value exhibited remarkably low (statistically undetectable) mutational variance, low micro-environmental variance, and high line survival over time, consistent with limited mutational decay in fitness. The three genotypes with detectable mutational input showed declines in mean size over time, indicating a consistent mutational bias toward smaller size, as reported in other taxa. The magnitude of this bias appeared genotype dependent, with the MA populations founded from the larger ancestors declining nearly twice as fast as that founded from the smallest ancestor. Together, these results demonstrate substantial heterogeneity in mutational properties among genotypes within a single natural population where the trait value spans a relatively narrow range. Such genotype-specific mutational input is expected to shape both the standing genetic variance and the evolutionary trajectory of polygenic traits.

Extreme climatic events are reshaping ecosystems worldwide as individual organisms vary markedly in their ability to withstand these disturbances. Deciphering patterns of persistence on local scales is therefore critical for predicting biodiversity trajectories under intensifying climate extremes. In this study, we examined variation in thermal stress responses among individuals of the coral Stylophora pistillata species complex during a heatwave at Heron Island Reef, Australia. More than half of the focal coral colonies died on the reef, and survival of coral fragments maintained under ex situ common thermal stress conditions was significantly correlated with the survival of their source colony. This demonstrates that survival differences result largely from biological factors rather than differential thermal exposure across reef habitats. Under common garden conditions, we observed striking differences in bleaching severity and survival times among three sympatric cryptic taxa and their highly host-specific symbiont community. Within the most locally common taxon, corals from historically warmer and more seasonally variable reef habitats seem more susceptible to bleaching, contrary to expectations. Together, these results reveal how biological differences among cryptic taxa and among individuals can shape coral responses during a heatwave and advance our understanding of coral vulnerability in a rapidly warming world.

Climate change is a growing threat to biodiversity, and the persistence of populations largely depends on their capacity to adapt to changing environmental conditions. Although there is an urgent need to forecast population adaptive potential, it is unclear how such predictions are affected by the genomic architectures underlying local adaptation across a species' range. In this study, we examine the genomic basis of local adaptation of the short-distance dispersing coral Stylophora pistillata, sampled at forty-six sites across eight reefs of the Great Barrier Reef, Australia. Our results show that thermal adaptation for this species involves hundreds of genomic loci with combinations that differ across regions. Although adaptive loci were largely region-specific, genotype-environment relationships estimated across the range provided sensible predictions of regional-level local adaptation. Additionally, predicted shifts in genotype-environment associations under increased projected warming were highly spatially variable, both between and within geographic regions. While some Great Barrier Reef S. pistillata populations might be well-adapted for near-future (2050) and moderate (SSP1-2.6 and SSP2-4.5) climate warming, up to 30% may face severe maladaptation risk by 2100 under a high-emission (SSP5-8.5) scenario. Collectively, these findings offer new insights into the spatial distribution of adaptive potential in coral populations and how it might shape their resilience in a warming ocean.

Infectious diseases present a growing risk to wildlife biodiversity. Predicting outbreak dynamics and developing effective management tools require knowledge on the mechanisms of infection transmission. Specifically, understanding the relative contributions of direct host-to-host transmission versus indirect environmental transmission is critical. Here, we leverage a large dataset from long-term monitoring of a free-living population of eastern water dragons (Intellagama lesueurii) experiencing an outbreak of the fungal pathogen Nannizziopsis barbatae to investigate this pathogen’s transmission. Using different host behaviours to model direct and indirect transmission of infection in this population, we demonstrate N. barbatae’s ability to infect hosts through indirect transmission. Our findings shed light on the danger N. barbatae poses to Australian reptiles but also provide insights into how outbreaks should be managed. Additionally, we provide a methodology to elucidate the transmission mechanisms of driving the spread of emerging fungal pathogens.

The distribution of pleiotropic mutational effects impacts phenotypic adaptation. However, small effect sizes and high sampling error of covariances hinder investigations of the factors influencing this distribution. Here, we explored the potential for shared information across traits affected by the same mutations to counter sampling error, allowing robust characterization of patterns of mutational input. Exploiting a published dataset representing 12 samples of the same mutation accumulation experiment in Drosophila serrata, we inferred robust signals of mutational effects from the concordance across samples. Krzanowski’s common subspace analysis identified a multivariate wing trait with statistically supported mutational variance in all samples. Importantly, this multivariate trait was aligned with the major axis of among-line (mutational) variance within most population samples. That is, despite considerable heterogeneity among samples in individual (co)variance parameter estimates, the predominant pattern of correlated mutational effects was identified in each dataset. 2 other multivariate traits were statistically supported across most samples. Smaller effect sizes (lower mutational variance) with concomitant larger sampling error or other factors (e.g., microenvironmental dependence of effects) may reduce the robustness of estimated mutational input for these traits. Overall, our results suggest that multivariate analyses of mutation accumulation experiments can detect the true signal of pleiotropic mutation, and that sampling error does not preclude such studies from extending our knowledge of pleiotropic mutational effects.

The distribution of pleiotropic mutational effects impacts phenotypic adaptation. However, small effect sizes and high sampling error of covariances hinder investigations of the factors influencing this distribution. Here, we explored the potential for shared information across traits affected by the same mutations to counter sampling error, allowing robust characterisation of patterns of mutational input. Exploiting a published dataset representing 12 samples of the same mutation accumulation experiment in Drosophila serrata , we inferred robust signals of mutational effects from the concordance across samples. Krzanowski common subspace analysis identified a multivariate wing trait with statistically supported mutational variance in all samples. Importantly, this multivariate trait was aligned with the major axis of among-line (mutational) variance within most population samples. That is, despite considerable heterogeneity among samples in individual (co)variance parameter estimates, the predominant pattern of correlated mutational effects was identified in datasets reflecting a typical mutation accumulation experimental design. Two other multivariate traits were statistically supported across most samples. Smaller effect sizes (lower mutational variance) with concomitant larger sampling error or other factors (e.g., microenvironmental dependence of effects) may reduce the robustness of estimated mutational input for these traits. Overall, our results suggest sampling error does not preclude multivariate analyses of mutation accumulation experiments from extending our knowledge of pleiotropic mutational effects.

In highly dispersive taxa, gene flow can homogenise genetic variation over broad spatial and temporal scales. However, phenotypic differentiation can still arise when heritable genetic variation is available to selection and (or) when organisms exhibit plasticity. Disentangling heritable versus non-heritable components of variation is possible using genomic animal models, but this approach has been underused in wild organisms. We investigated head shape variation in the marine cryptobenthic fish Bathygobius cocosensis, a highly dispersive species occupying heterogeneous environments. Head shape, a diet-related trait, is spatially structured in Australian populations. We curated a unique dataset comprising genotypic, phenotypic, and environmental variation to: (1) contrast the scales over which genetic and phenotypic variation are structured; and (2) quantify heritable versus non-heritable contributions to head shape variation using genomic animal models and comparisons between FST, PST, and QST. At macrogeographic scales (hundreds of kilometres) and over time (2 years), phenotypic differentiation (0.0001 ≤ PST ≤ 0.47) exceeded both genomic and additive genetic differentiation (0.001 ≤ FST ≤ 0.004 and 0.00001 ≤ QST ≤ 0.004, respectively). This suggests head shape variation may primarily reflect (non-heritable) plastic responses, rather than (heritable) adaptive genetic changes in mean head shape. At microgeographic scales, associations between head shape and tide pool variables were temporally variable, indicating that local environmental conditions may structure phenotypes within populations. Overall, this study highlights the value of genomic animal models for disentangling heritable and non-heritable components of phenotypic variation in dispersive marine taxa. It provides an integrative analysis linking genetic, phenotypic, and environmental variation in a cryptobenthic fish, highlighting how phenotypic divergence can emerge without strong genetic differentiation, and challenging the common assumption that phenotypic divergence necessarily implies adaptation.

The impact of selection on host immune function genes has been widely documented. However, it remains essentially unknown how mutation influences the quantitative immune traits that selection acts on. Applying a classical mutation accumulation (MA) experimental design in Drosophila serrata, we found the mutational variation in susceptibility (median time of death, LT50) to Drosophila C virus (DCV) was of similar magnitude to that reported for intrinsic survival traits. Mean LT50 did not change as mutations accumulated, suggesting no directional bias in mutational effects. Maintenance of genetic variance in immune function is hypothesised to be influenced by pleiotropic effects on immunity and other traits that contribute to fitness. To investigate this, we assayed female reproductive output for a subset of MA lines with relatively long or short survival times under DCV infection. Longer survival time tended to be associated with lower reproductive output, suggesting that mutations affecting susceptibility to DCV had pleiotropic effects on investment in reproductive fitness. Further studies are needed to uncover the general patterns of mutational effect on immune responses and other fitness traits, and to determine how selection might typically act on new mutations via their direct and pleiotropic effects.