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1. Fidelity varies in the symbiosis between a gutless marine worm and its microbial consortium

   https://doi.org/10.1186/s40168-022-01372-2  

   Sato, Yui ; Wippler, Juliane ; Wentrup, Cecilia ; Ansorge, Rebecca ; Sadowski, Miriam ; Gruber-Vodicka, Harald ; Dubilier, Nicole ; Kleiner, Manuel ( October 2022 , Microbiome)

   Many animals live in intimate associations with a species-rich microbiome. A key factor in maintaining these beneficial associations is fidelity, defined as the stability of associations between hosts and their microbiota over multiple host generations. Fidelity has been well studied in terrestrial hosts, particularly insects, over longer macroevolutionary time. In contrast, little is known about fidelity in marine animals with species-rich microbiomes at short microevolutionary time scales, that is at the level of a single host population. Given that natural selection acts most directly on local populations, studies of microevolutionary partner fidelity are important for revealing the ecological and evolutionary processes that drive intimate beneficial associations within animal species.

   In this study on the obligate symbiosis between the gutless marine annelidOlavius algarvensisand its consortium of seven co-occurring bacterial symbionts, we show that partner fidelity varies across symbiont species from strict to absent over short microevolutionary time. Using a low-coverage sequencing approach that has not yet been applied to microbial community analyses, we analysed the metagenomes of 80O. algarvensisindividuals from the Mediterranean and compared host mitochondrial and symbiont phylogenies based on single-nucleotide polymorphisms across genomes. Fidelity was highest for the two chemoautotrophic, sulphur-oxidizing symbionts that dominated the microbial consortium of allO. algarvensisindividuals. In contrast, fidelity was only intermediate to absent in the sulphate-reducing and spirochaetal symbionts with lower abundance. These differences in fidelity are likely driven by both selective and stochastic forces acting on the consistency with which symbionts are vertically transmitted.

   We hypothesize that variable degrees of fidelity are advantageous forO. algarvensisby allowing the faithful transmission of their nutritionally most important symbionts and flexibility in the acquisition of other symbionts that promote ecological plasticity in the acquisition of environmental resources.

    

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2. Host–enemy interactions provide limited biotic resistance for a range‐expanding species via reduced apparent competition

   https://doi.org/10.1111/ddi.13763  

   Prior, Kirsten M. ; Jones, Dylan G. ; Meadley‐Dunphy, Shannon A. ; Lee, Susan ; Milks, Alyson K. ; Daughton, Sage ; Forbes, Andrew A. ; Powell, Thomas H. Q. ( August 2023 , Diversity and Distributions)

   As species' ranges shift poleward in response to anthropogenic change, they may lose antagonistic interactions if they move into less diverse communities, fail to interact with novel populations or species effectively, or if ancestral interacting populations or species fail to shift synchronously. We leveraged a poleward range expansion in a tractable insect host–enemy community to uncover mechanisms by which altered antagonistic interactions between native and recipient communities contributed to ‘high niche opportunities’ (limited biotic resistance) for a range‐expanding insect.

   North America, Pacific Northwest.

   We created quantitative insect host–enemy interaction networks by sampling oak gall wasps on 400 trees of a dominant oak species in the native and expanded range of a range‐expanding gall wasp species. We compared host–enemy network structure between regions. We measured traits (phenology, morphology) of galls and interacting parasitoids, predicting greater trait divergence in the expanded range. We measured function relating to host control and explored if altered interactions and traits contributed to reduced function, or biotic resistance.

   Interaction networks had fewer species in the expanded range and lower complementarity of parasitoid assemblages among host species. While networks were more generalized, interactions with the range‐expanding species were more specialized in the expanded range. Specialist enemies effectively tracked the range‐expanding host, and there was reduced apparent competition with co‐occurring hosts by shared generalist enemies. Phenological divergence of enemy assemblages interacting with the range‐expanding and co‐occurring hosts was greater in the expanded range, potentially contributing to weak apparent competition. Biotic resistance was lower in the expanded range, where fewer parasitoids emerged from galls of the range‐expanding host.

   Changes in interactions with generalist enemies created high niche opportunities, and limited biotic resistance, suggesting weak apparent competition may be a mechanism of enemy release for range‐expanding insects embedded within generalist enemy networks.

    

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3. Discordant population structure among rhizobium divided genomes and their legume hosts

   https://doi.org/10.1111/mec.16704  

   Riley, Alex B. ; Grillo, Michael A. ; Epstein, Brendan ; Tiffin, Peter ; Heath, Katy D. ( October 2022 , Molecular Ecology)

   Symbiosis often occurs between partners with distinct life history characteristics and dispersal mechanisms. Many bacterial symbionts have genomes comprising multiple replicons with distinct rates of evolution and horizontal transmission. Such differences might drive differences in population structure between hosts and symbionts and among the elements of the divided genomes of bacterial symbionts. These differences might, in turn, shape the evolution of symbiotic interactions and bacterial evolution. Here we use whole genome resequencing of a hierarchically structured sample of 191 strains ofSinorhizobium meliloticollected from 21 locations in southern Europe to characterize population structures of this bacterial symbiont, which forms a root nodule symbiosis with the host plantMedicago truncatula.S. melilotigenomes showed high local (within‐site) variation and little isolation by distance. This was particularly true for the two symbiosis elements, pSymA and pSymB, which have population structures that are similar to each other, but distinct from both the bacterial chromosome and the host plant. Given limited recombination on the chromosome, compared to the symbiosis elements, distinct population structures may result from differences in effective gene flow. Alternatively, positive or purifying selection, with little recombination, may explain distinct geographical patterns at the chromosome. Discordant population structure between hosts and symbionts indicates that geographically and genetically distinct host populations in different parts of the range might interact with genetically similar symbionts, potentially minimizing local specialization.

    

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4. Novel insights into symbiont population structure: Globe‐trotting avian feather mites contradict the specialist–generalist variation hypothesis

   https://doi.org/10.1111/mec.17115  

   Matthews, Alix E. ; Boves, Than J. ; Sweet, Andrew D. ; Ames, Elizabeth M. ; Bulluck, Lesley P. ; Johnson, Erik I. ; Johnson, Matthew ; Lipshutz, Sara E. ; Percy, Katie L. ; Raybuck, Douglas W. ; et al ( August 2023 , Molecular Ecology)

   Researchers often examine symbiont host specificity as a species‐level pattern, but it can also be key to understanding processes occurring at the population level, which are not as well understood. The specialist–generalist variation hypothesis (SGVH) attempts to explain how host specificity influences population‐level processes, stating that single‐host symbionts (specialists) exhibit stronger population genetic structure than multi‐host symbionts (generalists) because of fewer opportunities for dispersal and more restricted gene flow between populations. However, this hypothesis has not been tested in systems with highly mobile hosts, in which population connectivity may vary temporally and spatially. To address this gap, we tested the SGVH on proctophyllodid feather mites found on migratory warblers (family Parulidae) with contrasting host specificities,Amerodectes protonotaria(a host specialist ofProtonotaria citrea) andA. ischyros(a host generalist of 17 parulid species). We used a pooled‐sequencing approach and a novel workflow to analyse genetic variants obtained from whole genome data. Both mite species exhibited fairly weak population structure overall, and contrary to predictions of the SGVH, the generalist was more strongly structured than the specialist. These results may suggest that specialists disperse more freely among conspecifics, whereas generalists sort according to geography. Furthermore, our results may reflect an unexpected period for mite transmission – during the nonbreeding season of migratory hosts – as mite population structure more closely reflects the distributions of hosts during the nonbreeding season. Our findings alter our current understanding of feather mite biology and highlight the potential for studies to explore factors driving symbiont diversification at multiple evolutionary scales.

    

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5. A Phylogeny-Informed Analysis of the Global Coral-Symbiodiniaceae Interaction Network Reveals that Traits Correlated with Thermal Bleaching Are Specific to Symbiont Transmission Mode

   https://doi.org/10.1128/mSystems.00266-21  

   Swain, Timothy D. ; Lax, Simon ; Gilbert, Jack ; Backman, Vadim ; Marcelino, Luisa A. ( June 2021 , mSystems)

   Bik, Holly (Ed.)

   ABSTRACT The complex network of associations between corals and their dinoflagellates (family Symbiodiniaceae) are the basis of coral reef ecosystems but are sensitive to increasing global temperatures. Coral-symbiont interactions are restricted by ecological and evolutionary determinants that constrain partner choice and influence holobiont response to environmental stress; however, little is known about how these processes shape thermal resilience of the holobiont. Here, we built a network of global coral-Symbiodiniaceae associations, mapped species traits (e.g., symbiont transmission mode and biogeography) and phylogenetic relationships of both partners onto the network, and assigned thermotolerance to both host and symbiont nodes. Using network analysis and phylogenetic comparative methods, we determined the contribution of species traits to thermal resilience of the holobiont, while accounting for evolutionary patterns among species. We found that the network shows nonrandom interactions among species, which are shaped by evolutionary history, symbiont transmission mode (horizontally transmitted [HT] or vertically transmitted [VT] corals) and biogeography. Coral phylogeny, but not Symbiodiniaceae phylogeny, symbiont transmission mode, or biogeography, was a good predictor of thermal resilience. Closely related corals have similar Symbiodiniaceae interaction patterns and bleaching susceptibilities. Nevertheless, the association patterns that explain increased host thermal resilience are not generalizable across the entire network but are instead unique to HT and VT corals. Under nonstress conditions, thermally resilient VT coral species associate with thermotolerant phylotypes and limit their number of unique symbionts and overall symbiont thermotolerance diversity, while thermally resilient HT coral species associate with a few host-specific symbiont phylotypes. IMPORTANCE Recent advances have revealed a complex network of interactions between coral and Symbiodiniaceae. Specifically, nonrandom association patterns, which are determined in part by restrictions imposed by symbiont transmission mode, increase the sensitivity of the overall network to thermal stress. However, little is known about the extent to which coral-Symbiodiniaceae network resistance to thermal stress is shaped by host and symbiont species phylogenetic relationships and host and symbiont species traits, such as symbiont transmission mode. We built a frequency-weighted global coral-Symbiodiniaceae network and used network analysis and phylogenetic comparative methods to show that evolutionary relatedness, but not transmission mode, predicts thermal resilience of the coral-Symbiodiniaceae holobiont. Consequently, thermal stress events could result in nonrandom pruning of susceptible lineages and loss of taxonomic diversity with catastrophic effects on community resilience to future events. Our results show that inclusion of the contribution of evolutionary and ecological processes will further our understanding of the fate of coral assemblages under climate change. 

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