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Biology subjects

Popovic, I.

Publications and source records attributed to Popovic, I..

9 recordsLinked to original sources

Heatwave winners and losers: cryptic coral holobionts differ in thermal tolerance

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.

ecology↗

Localised admixture triggers parallel adaptation in a coral species trio on the Great Barrier Reef

Hybridisation can shape evolutionary trajectories and fuel rapid adaptation. Yet, whether adaptive introgression repeatedly reconfigures genomes in predictable ways remains largely unknown. Here, we show that three-way admixture drives repeatable parallel differentiation in reef-building corals in the Acropora hyacinthus species complex. Adaptive introgression is confined to the southern Great Barrier Reef, where admixture timing coincides with a recent breakdown in species barriers despite limited historical gene flow. Genome-wide introgression is characterised by numerous shared minor-parent ancestry peaks that are enriched for stress-response genes and under positive selection for parallel adaptive admixture. Our results demonstrate that introgressive hybridisation can be geographically restricted between sympatric marine species and can promote repeated rapid adaptation that transcends species boundaries.

evolutionary biology↗

Genomic repeatability and predictability of local (mal)adaptation in a reef-building coral

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 local 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 geographic regions. Although adaptive loci were largely region-specific, genotype-environment relationships estimated across the entire range could predict regional-level adaptive patterns. This shows that genome-wide sequence data combined with geographically broad sampling can support reliable evolutionary forecasting. Under climate change projections, predicted shifts in genotype-environment associations were highly spatially variable, both between and within geographic regions. While some populations might be sufficiently adapted for moderate (SSP1-2.6 and SSP2-4.5) climate warming by 2050, 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 coral adaptive potential and how it might shape corals resilience in a warming ocean.

evolutionary biology↗

Causal modelling reveals lower coral genetic diversity in more heterogenous reef environments

Conserving genetic diversity is crucial for maintaining species evolutionary potential and resilience to environmental change. Yet, directly measuring genetic diversity across large spatial scales remains resource-intensive and impractical for conservation planning. Identifying reliable, accessible, and cost-effective spatial predictors of genetic diversity would significantly enhance our ability to incorporate genetic diversity into conservation efforts. Caribbean coral reefs represent a compelling system for investigating such predictors, as these ecosystems face unprecedented threats from disease outbreaks and climate change. Here, we investigate the utility of several environmental proxies as surrogates for genetic diversity, which may be useful for conservation planning in resource- or data-poor regions. To achieve this goal, we used reduced-representation genomic sequencing to estimate intraspecific genetic diversity, and in doing so, identified two genetically distinct and sympatric cryptic coral species in the Agaricia tenuifolia species complex. We employed a causal inference approach to assess the relationships between genetic alpha diversity and habitat area and connectivity, habitat heterogeneity, and temperature. Statistical investigations revealed that increased habitat heterogeneity, derived from remotely sensed habitat maps, was associated with lower genetic diversity within coral populations, suggesting that habitat characteristics promoting species diversity may not maintain high genetic diversity within a single species. Habitat area and connectivity, and temperature have predominantly negative effects on genetic diversity with coral habitat area and connectivity showing markedly contrasting responses in two cryptic taxa. Thus, our findings reveal that context matters greatly, as results differ between cryptic species, across variables, and among spatial scales.

evolutionary biology↗

Long-distance gene flow and contrasting population structures of reef-building corals and their algal symbionts inform adaptive potential across the Western Pacific

The genetic diversity and connectivity of reef-building coral populations are key to their survival in warming oceans. Yet our understanding of corals demographic resilience and adaptive potential is complicated by cryptic species diversity, wide geographic distributions, and complex coral-algal symbioses. To address these challenges, we investigated genetic connectivity and diversity of the broadcast-spawning coral Acropora spathulata and its associated Symbiodiniaceae across 29 reefs spanning the Great Barrier Reef, the Coral Sea, and New Caledonia, using whole-genome sequencing of 1,088 colonies. We identified four genetically distinct coral populations that diverged between 0.27 and 0.65 million years ago, likely due to geographic isolation across thousands of kilometers. These populations maintained asymmetrical gene flow along major ocean currents despite demographic isolation, and sustained large local effective population sizes ([~]2,900), supported by a high dispersal range of [~]100 km per generation. In contrast, their Symbiodiniaceae partners varied over finer spatial scales, with five distinct Cladocopium taxa distributed along latitudinal and cross-shore gradients, likely driven by local environmental conditions. These results suggest that high dispersal capacity and large local population size promote demographic resilience within reef systems, while environment-specific symbioses and long-distance gene flow across reef-systems support adaptation and evolutionary rescue.

molecular biology↗

Proximity and current alignment drives fertilisation success in a broadcast-spawning coral

As coral populations decline under climate change and other stressors, surviving corals will become increasingly isolated. While Allee effects that reduce gamete encounters and fertilisation success may lead to reproductive and recruitment failure, the critical population densities and distances between individuals required to maintain viable populations remains uncertain. Here, we investigate the links between colony isolation and fertilisation patterns using an experimentally manipulated patch of the broadcast spawning tabular coral, Acropora hyacinthus. Corals were arranged in a clustered radial design, with colonies arranged at increasing distances radiating downstream from a central spawning aggregation. Fertilisation and paternity assignment analyses were used to examine the influence of parental distance, current alignment, colony size, and genetic relatedness. Fertilisation success declined sharply with increasing distance among corals, and paternity assignments indicated most parents were located within 3 m of each other, underscoring the importance of colony proximity. Additionally, fertilisation success was highest for colonies positioned downstream of the central cluster, and 84% of sequenced progeny were sired by colonies located directly upstream. Simulations of natural reef spatial population distributions projected onto a virtual grid, incorporating empirically derived parentage distances, indicated that populations remained well-mixed at typical adult densities in nearby reefs. However, as densities decreased to 1 colony per 100 m-2 (i.e. 0.01 colonieslllm-2), reproductive isolation and the formation of patchy breeding units became prevalent. Overall, our findings highlight that the spatial arrangement and isolation of corals on reefs, and subsequent Allee effects on fertilisation, can jeopardise the reproductive success of broadcast spawning corals. Conservation efforts are needed to help maintain viable coral populations and successful reproductive aggregations for degraded reef systems.

ecology↗

Environmental, host, and symbiont drivers of heat tolerance in a species complex of reef-building corals

Reef-building coral populations are under unprecedented threat from climate warming. Yet, variation in coral heat tolerance exists whereby some colonies can cope with higher sea temperatures than others and thus may hold unique value for conservation and restoration. Here, we quantify variation in heat tolerance of an ecologically important tabular coral species complex across the Great Barrier Reef (GBR) while also measuring genomic variation in the coral host and symbiont partners. Coral bleaching and photochemical traits were measured in 569 colonies within the Acropora hyacinthus species complex from 17 reefs following exposure to standardized acute heat stress assays. We detected substantial variation in heat tolerance, where individual colony thermal thresholds differed by up to 7.3{degrees}C and 5.7{degrees}C among and within reefs, respectively. Sea surface temperature climatology was the strongest predictor of heat tolerance, where colonies from warmer northern and inshore reefs typically exhibited the highest thermal thresholds, while colonies from cooler southern reefs were able to tolerate greater temperature increases relative to their local summer temperatures. Heat tolerance was also positively associated with exposure to thermal stress in the weeks preceding measurements. Assignment of colonies to host genomic clusters revealed four putative species within the A. hyacinthus complex that did not vary in their responses to experimental heat stress. Symbiodiniaceae communities within colonies were comprised primarily of Cladocopium ITS2 variants that differed spatially but had minimal effect on heat tolerance. Between 36 - 80% of heat tolerance variation was explained by environmental, host, and symbiont genomic predictors, leaving 20 - 64% to be explained by additional underlying drivers such as functional genomic variation not measured here. These results may be used to inform conservation and restoration actions, including targeting heat tolerant individuals for selective breeding, and will provide a foundation for evaluating the genomic basis of heat tolerance.

ecology↗

High germline mutation rates but not extreme population size outbreaks influence genetic diversity in crown-of-thorns sea stars

Lewontins paradox, the observation that levels of genetic diversity ({pi}) among animals do not scale linearly with variation in census population sizes (Nc), is an evolutionary conundrum, where the most extreme mismatches between {pi} and Nc are found for highly abundant marine invertebrates. Yet, whether new mutations influence {pi} relative to extrinsic processes remains unknown for most taxa. Here, we provide the first direct germline mutation rate () estimate for a marine invertebrate, using high-coverage (60x) whole-genome sequencing of wild-caught Acanthaster cf. solaris crown-of-thorns sea stars (Echinodermata). We also provide empirical estimates of adult Nc in Australias Great Barrier Reef to jointly examine the determinants of {pi}. Based on direct observations of 63 de novo mutations across 14 parent-offspring trios, the A. cf. solaris mean was 9.13 x 10-09 mutations per-site per-generation (95% CI: 6.51 x 10-09 to 1.18 x 10-08). This value exceeds estimates for other invertebrates, showing greater concordance with reported vertebrate germline mutation rates. Lower-than-expected Ne ([~]70,000-180,000) and low Ne/Nc values (0.0047-0.048) indicated significant genetic drift and weak influences of contemporary population outbreaks on long-term {pi}. Our findings of elevated and low Ne in A. cf. solaris may help explain high mutational loads and extreme polymorphism levels observed in some marine invertebrate taxa and are consistent with evolving in response to Ne (drift-barrier hypothesis). This study advances our understanding of the processes controlling levels of natural genetic variation and provides new data valuable for further testing hypotheses about mutation rate evolution across animal phyla.

evolutionary biology↗

DILS : Demographic Inferences with Linked Selection by using ABC

We present DILS, a deployable statistical analysis platform for conducting demographic inferences with linked selection from population genomic data using an Approximate Bayesian Computation framework. DILS takes as input single-population or two-population datasets (multilocus fasta sequences) and performs three types of analyses in a hierarchical manner, identifying: 1) the best demographic model to study the importance of gene flow and population size change on the genetic patterns of polymorphism and divergence, 2) the best genomic model to determine whether the effective size Ne and migration rate N.m are heterogeneously distributed along the genome (implying linked selection) and 3) loci in genomic regions most associated with barriers to gene flow. Also available via a web interface, an objective of DILS is to facilitate collaborative research in speciation genomics. Here, we show the performance and limitations of DILS by using simulations, and finally apply the method to published data on a divergence continuum composed by 28 pairs of Mytilus mussel populations/species.

evolutionary biology↗