Growth of brown trout in the wild predicted by embryo stress reaction in the laboratory

Laboratory studies on embryos of salmonids, such as the brown trout (Salmo trutta), have been extensively used to study environmental stress and how responses vary within and between natural populations. These studies are based on the implicit assumption that early life-history traits are relevant for stress tolerance in the wild. Here we test this assumption by combining two datasets from studies on the same 60 full-sib families. These families had been experimentally produced from wild breeders to determine, in separate samples, (i) stress tolerances of singly kept embryos in the laboratory and (ii) growth of juveniles during 6 months in the wild. We found that growth in the wild was well predicted by larval size of their full sibs in the laboratory, especially if these siblings had been experimentally exposed to a pathogen. Exposure to the pathogen had not caused elevated mortality among the embryos but induced early hatching. The strength of this stress-induced change of life history was a significant predictor of juvenile growth in the wild: the stronger the response in the laboratory, the slower the growth in the wild. We conclude that embryo performance in controlled environments can be useful predictors of juvenile performance in the wild

Natural experiments and long-term monitoring are critical to understand and predict marine host-microbe ecology and evolution

© The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Leray, M., Wilkins, L. G. E., Apprill, A., Bik, H. M., Clever, F., Connolly, S. R., De Leon, M. E., Duffy, J. E., Ezzat, L., Gignoux-Wolfsohn, S., Herre, E. A., Kaye, J. Z., Kline, D. I., Kueneman, J. G., McCormick, M. K., McMillan, W. O., O’Dea, A., Pereira, T. J., Petersen, J. M., Petticord, D. F., Torchin, M. E., Thurber, R. V., Videvall, E., Wcislo, W. T., Yuen, B., Eisen, J. A. . Natural experiments and long-term monitoring are critical to understand and predict marine host-microbe ecology and evolution. Plos Biology, 19(8), (2021): e3001322, https://doi.org/10.1371/journal.pbio.3001322.Marine multicellular organisms host a diverse collection of bacteria, archaea, microbial eukaryotes, and viruses that form their microbiome. Such host-associated microbes can significantly influence the host’s physiological capacities; however, the identity and functional role(s) of key members of the microbiome (“core microbiome”) in most marine hosts coexisting in natural settings remain obscure. Also unclear is how dynamic interactions between hosts and the immense standing pool of microbial genetic variation will affect marine ecosystems’ capacity to adjust to environmental changes. Here, we argue that significantly advancing our understanding of how host-associated microbes shape marine hosts’ plastic and adaptive responses to environmental change requires (i) recognizing that individual host–microbe systems do not exist in an ecological or evolutionary vacuum and (ii) expanding the field toward long-term, multidisciplinary research on entire communities of hosts and microbes. Natural experiments, such as time-calibrated geological events associated with well-characterized environmental gradients, provide unique ecological and evolutionary contexts to address this challenge. We focus here particularly on mutualistic interactions between hosts and microbes, but note that many of the same lessons and approaches would apply to other types of interactions.Financial support for the workshop was provided by grant GBMF5603 (https://doi.org/10.37807/GBMF5603) from the Gordon and Betty Moore Foundation (W.T. Wcislo, J.A. Eisen, co-PIs), and additional funding from the Smithsonian Tropical Research Institute and the Office of the Provost of the Smithsonian Institution (W.T. Wcislo, J.P. Meganigal, and R.C. Fleischer, co-PIs). JP was supported by a WWTF VRG Grant and the ERC Starting Grant 'EvoLucin'. LGEW has received funding from the European Union’s Framework Programme for Research and Innovation Horizon 2020 (2014-2020) under the Marie Sklodowska-Curie Grant Agreement No. 101025649. AO was supported by the Sistema Nacional de Investigadores (SENACYT, Panamá). A. Apprill was supported by NSF award OCE-1938147. D.I. Kline, M. Leray, S.R. Connolly, and M.E. Torchin were supported by a Rohr Family Foundation grant for the Rohr Reef Resilience Project, for which this is contribution #2. This is contribution #85 from the Smithsonian’s MarineGEO and Tennenbaum Marine Observatories Network.

Introducing the Mangrove Microbiome Initiative: Identifying Microbial Research Priorities and Approaches To Better Understand, Protect, and Rehabilitate Mangrove Ecosystems

Mangrove ecosystems provide important ecological benefits and ecosystem services, including carbon storage and coastline stabilization, but they also suffer great anthropogenic pressures. Microorganisms associated with mangrove sediments and the rhizosphere play key roles in this ecosystem and make essential contributions to its productivity and carbon budget. Understanding this nexus and moving from descriptive studies of microbial taxonomy to hypothesis-driven field and lab studies will facilitate a mechanistic understanding of mangrove ecosystem interaction webs and open opportunities for microorganism-mediated approaches to mangrove protection and rehabilitation. Such an effort calls for a multidisciplinary and collaborative approach, involving chemists, ecologists, evolutionary biologists, microbiologists, oceanographers, plant scientists, conservation biologists, and stakeholders, and it requires standardized methods to support reproducible experiments. Here, we outline the Mangrove Microbiome Initiative, which is focused around three urgent priorities and three approaches for advancing mangrove microbiome research

MolEcol gene exp data

Gene expression of G6PD, GAPDH, MHCa of whitefish embryos that had been exposed to one of several treatment conditions. "Female" and "Male" give the mother and father, respectively

MolEcol Dead and Hatch data

Embryo survival and day of hatching. Each line represents one singly reared embryo exposed to one of the treatments. "Female" and "Male" give the embryo's mother and father, respectively

Data from: Effects of host genetics and environment on egg-associated microbiotas in brown trout (Salmo trutta)

Recent studies found fish egg-specific bacterial communities that changed over the course of embryogenesis, suggesting an interaction between the developing host and its microbiota. Indeed, single-strain infections demonstrated that the virulence of opportunistic bacteria is influenced by environmental factors and host immune genes. However, the interplay between a fish embryo host and its microbiota has not been studied yet at the community level. To test whether host genetics affects the assemblage of egg-associated bacteria, adult brown trout (Salmo trutta) were sampled from a natural population. Their gametes were used for full-factorial in vitro fertilizations to separate sire from dam effects. In total, 2520 embryos were singly raised under experimental conditions that differently support microbial growth. High-throughput 16S rRNA amplicon sequencing was applied to characterize bacterial communities on milt and fertilized eggs across treatments. Dam and sire identity influenced embryo mortality, time until hatching and composition of egg-associated microbiotas, but no link between bacterial communities on milt and on fertilized eggs could be found. Elevated resources increased embryo mortality and modified bacterial communities with a shift in their putative functional potential. Resource availability did not significantly affect any parental effects on embryo performance. Sire identity affected bacterial diversity that turned out to be a significant predictor of hatching time: embryos associated with high bacterial diversity hatched later. We conclude that both host genetics and the availability of resources define diversity and composition of egg-associated bacterial communities that then affect the life history of their hosts

Data from: MHC class I expression dependent on bacterial infection and parental factors in whitefish embryos (Salmonidae)

Ecological conditions can influence not only the expression of a phenotype, but also the heritability of a trait. As such, heritable variation for a trait needs to be studied across environments. We have investigated how pathogen challenge affects the expression of MHC genes in embryos of the lake whitefish Coregonus palaea. In order to experimentally separate paternal (i.e. genetic) from maternal and environmental effects, and determine whether and how stress affects the heritable variation for MHC expression, embryos were produced in full-factorial in vitro fertilizations, reared singly, and exposed at 208 degree days (late-eyed stage) to either one of two strains of Pseudomonas fluorescens that differ in their virulence characteristics (one increased mortality, while both delayed hatching time). Gene expression was assessed 48 h postinoculation, and virulence effects of the bacterial infection were monitored until hatching. We found no evidence of MHC class II expression at this stage of development. MHC class I expression was markedly down-regulated in reaction to both pseudomonads. While MHC expression could not be linked to embryo survival, the less the gene was expressed, the earlier the embryos hatched within each treatment group, possibly due to trade-offs between immune function and developmental rate or further factors that affect both hatching timing and MHC expression. We found significant additive genetic variance for MHC class I expression in some treatments. That is, changes in pathogen pressures could induce rapid evolution in MHC class I expression. However, we found no additive genetic variance in reaction norms in our study population

MolEcol Dead and Hatch data

Embryo survival and day of hatching. Each line represents one singly reared embryo exposed to one of the treatments. "Female" and "Male" give the embryo's mother and father, respectively

Data from: Environmental stress linked to consumption of maternally derived carotenoids in brown trout embryos (Salmo trutta)

The yellow, orange, or red colors of salmonid eggs are due to maternally derived carotenoids whose functions are not sufficiently understood yet. Here, we studied the significance of naturally acquired carotenoids as maternal environmental effects during embryo development in brown trout (Salmo trutta). We collected eggs from wild females, quantified their egg carotenoid content, fertilized them in vitro in full-factorial breeding blocks to separate maternal from paternal effects, and raised 3,278 embryos singly at various stress conditions until hatching. We found significant sire effects that revealed additive genetic variance for embryo survival and hatching time. Dam effects were 5.4 times larger than these sire effects, indicating that maternal environmental effects play an important role in determining embryo stress tolerance. Of the eight pigment molecules that we targeted, only astaxanthin, zeaxanthin (that both affected egg redness), and lutein were detected above our confidence thresholds. No strong link could be observed between carotenoid content in unfertilized eggs and embryo mortality or hatching timing. However, the consumption of carotenoids during our stress treatment was negatively correlated to embryo survival among sib groups and explained about 14% of the maternal environmental variance. We conclude that maternally derived carotenoids play a role in the ability of embryos to cope with environmental stress, but that the initial susceptibility to the organic pollution was mainly determined by other factors