Symbiont community diversity is more constrained in holobionts that tolerate diverse stressors

Howe‐Kerr, Lauren I.; Bachelot, Bénédicte; Wright, Rachel M.; Kenkel, Carly D.; Bay, Line K.; Correa, Adrienne M. S.

doi:10.1101/572479

Cited by 4 publications

(5 citation statements)

References 63 publications

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“…Another consideration is the contribution of the algal symbiont toward holobiont health. In this study, colonies primarily hosted Cladocopium symbionts almost exclusively, but also contained lower abundances of Brevolium, Durusdinium, and/or Gerakladinium symbionts (<0.1% of the total community; Howe- Kerr et al, 2019).…”

Section: Best Performing Genets Tolerate Multiple Stressorsmentioning

confidence: 64%

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Positive genetic associations among fitness traits support evolvability of a reef‐building coral under multiple stressors

Wright

Mera

Kenkel

et al. 2019

Global Change Biology

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Climate change threatens organisms in a variety of interactive ways that requires simultaneous adaptation of multiple traits. Predicting evolutionary responses requires an understanding of the potential for interactions among stressors and the genetic variance and covariance among fitness‐related traits that may reinforce or constrain an adaptive response. Here we investigate the capacity of Acropora millepora, a reef‐building coral, to adapt to multiple environmental stressors: rising sea surface temperature, ocean acidification, and increased prevalence of infectious diseases. We measured growth rates (weight gain), coral color (a proxy for Symbiodiniaceae density), and survival, in addition to nine physiological indicators of coral and algal health in 40 coral genets exposed to each of these three stressors singly and combined. Individual stressors resulted in predicted responses (e.g., corals developed lesions after bacterial challenge and bleached under thermal stress). However, corals did not suffer substantially more when all three stressors were combined. Nor were trade‐offs observed between tolerances to different stressors; instead, individuals performing well under one stressor also tended to perform well under every other stressor. An analysis of genetic correlations between traits revealed positive covariances, suggesting that selection to multiple stressors will reinforce rather than constrain the simultaneous evolution of traits related to holobiont health (e.g., weight gain and algal density). These findings support the potential for rapid coral adaptation under climate change and emphasize the importance of accounting for corals’ adaptive capacity when predicting the future of coral reefs.

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Section: Best Performing Genets Tolerate Multiple Stressorsmentioning

confidence: 64%

“…The final total genets for each sampling location are as follows: Davies ( n = 10), Rib ( n = 10), Pandora ( n = 14), and Esk ( n = 6). Algal symbiont types were investigated by ITS‐2 sequencing for eight of the coral colonies (Howe‐Kerr et al, ).…”

Section: Methodsmentioning

confidence: 99%

Positive genetic associations among fitness traits support evolvability of a reef‐building coral under multiple stressors

Wright

Mera

Kenkel

et al. 2019

Global Change Biology

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“…The physiological performance of corals can be significantly affected by their Symbiodiniaceae community composition (Oliver and Palumbi, 2011;Palumbi et al, 2014;Howe-Kerr et al, 2019;Eckert et al, 2020). Here, we found that Symbiodiniaceae community composition was associated with the interaction of the amount of weight gained and transplant location at the Gardens site, and may also have contributed to heat tolerance.…”

Section: Discussionmentioning

confidence: 64%

Signatures of Adaptation and Acclimatization to Reef Flat and Slope Habitats in the Coral Pocillopora damicornis

et al. 2021

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Strong population-by-habitat interactions across environmental gradients arise from genetic adaptation or acclimatization and represents phenotypic variation required for populations to respond to changing environmental conditions. As such, patterns of adaptation and acclimatization of reef-building corals are integral to predictions of the future of coral reefs under climate warming. The common brooding coral, Pocillopora damicornis, exhibits extensive differences in host genetic and microbial symbiont community composition between depth habitats at Heron Island in the southern Great Barrier Reef, Australia. An 18-month reciprocal field transplant experiment was undertaken to examine the environmental and genetic drivers behind variation in survival, weight gain, heat tolerance and algal symbiont community between the reef flat and slope habitats. We observed population-by-habitat interactions for in situ partial mortality and weight gain, where trait-related fitness of natives was greater than transplants in most cases, consistent with local adaptation. On average, flat colonies transplanted to the slope had a relatively low partial mortality but minimal weight gain, whereas slope colonies transplanted to the flat had relatively high partial mortality and average weight gain. Experimental heat tolerance was always higher in colonies sourced from the flat, but increased when slope colonies were transplanted to the flat, providing evidence of acclimatization in these colonies. The performance of certain slope to flat transplants may have been driven by each colony’s algal symbiont (Symbiodiniaceae) community, and flat variants were observed in a small number of slope colonies that either had a fixed flat composition before transplantation or shuffled after transplantation. Host genotypes of previously identified genetic outlier loci could not predict survival following transplantation, possibly because of low sample size and/or polygenic basis to the traits examined. Local environmental conditions and Symbiodiniaceae composition may provide insight into the adaptive potential to changing environmental conditions.

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“…However, it is also possible that a symbiont that translocates less material might end up becoming specialized for a particular host before a "better" symbiont partner could become entrained in the host's biology. Recent observations that more diverse symbiont communities are found in holobionts less resistant to environmental stressors (Howe-Kerr et al, 2020) might be explained by a lack of tight specialization between host and symbiont.…”

Section: General Observationsmentioning

confidence: 99%

Sustained beneficial infections: priority effects, competition, and specialization drive patterns of association in intracellular mutualisms

Hill,

Lawson,

Cain

et al. 2023

Front. Ecol. Evol.

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Intracellular symbioses provide a useful system for exploring evolutionary and ecological forces that shape mutualistic partnerships. Within- and among-host competitiveness driven by different strategies that symbionts adopt as they transfer materials to the host across a sub-cellular membrane might explain patterns of host:symbiont association observed in natural systems. We tested the hypothesis that different translocation strategies employed by symbionts affect their ability to occupy host habitats using two distinct modeling approaches. The first involved constructing a deterministic, Lotka-Volterra-type model with two symbiont species competing for access to a single host. The model recovered expected behaviors of co-occupancy/coinfection as well as competitive exclusion. However, a specialization coefficient allowed advantages to accrue to one of the symbionts and permitted otherwise inferior competitors to displace superior competitors. The second approach involved developing and implementing a detailed, highly configurable, and realstic agent-based model (ABM), facilitating experimentation of multiple symbiont strategies in competition simultaneously. The ABM emphasizes bidirectional movement of materials between symbiont and host (e.g., photosynthate from algae to heterotrophic host). Competitive interactions between symbionts based on simple strategies led to exclusion of the inferior symbiont or co-occupancy of the host. As in the first model, inferior competitors could overtake superior competitors when “affinity” terms (i.e., specialization) were included in the model. Both models lay bare the importance of coevolutionary specialization as a selectively advantageous strategy, and they offer a new conceptual framework for interpreting the dynamic patterns observed in extant host and mutualist associations by challenging the idea of “host control” of outcomes, and identifying specific points where coevolutionary specialization might accrue.

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Symbiont community diversity is more constrained in holobionts that tolerate diverse stressors

Cited by 4 publications

References 63 publications

Positive genetic associations among fitness traits support evolvability of a reef‐building coral under multiple stressors

Positive genetic associations among fitness traits support evolvability of a reef‐building coral under multiple stressors

Signatures of Adaptation and Acclimatization to Reef Flat and Slope Habitats in the Coral Pocillopora damicornis

Sustained beneficial infections: priority effects, competition, and specialization drive patterns of association in intracellular mutualisms

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