Symbiont specificity, both at the phylotype and strain level, can have profound consequences for host ecology and evolution. However, except for insights from a few model symbiosis systems, the degree of partner fidelity and the influence of host versus environmental factors on symbiont composition are still poorly understood. Nutritional symbioses between invertebrate animals and chemosynthetic bacteria at deep-sea hydrothermal vents are examples of relatively selective associations, where hosts affiliate only with particular, environmentally acquired phylotypes of gammaproteobacterial or campylobacterial symbionts. In hydrothermal vent snails of the sister genera Alviniconcha and Ifremeria , this phylotype specificity has been shown to play a role in habitat distribution and partitioning among different holobiont species. However, it is currently unknown if fidelity goes beyond species-level associations and influences genetic structuring, connectivity, and habitat adaptation of holobiont populations. We used metagenomic analyses to assess sequence variation in hosts and symbionts and identify correlations with geographic and environmental factors. Our analyses indicate that host populations are not differentiated across an ∼800-km gradient, while symbiont populations are clearly structured between vent locations due to a combination of neutral and selective processes. Overall, these results suggest that host individuals flexibly associate with locally adapted strains of their specific symbiont phylotypes, which supports a long-standing but untested paradigm of the benefits of horizontal transmission. Symbiont strain flexibility in these snails likely enables host populations to exploit a range of habitat conditions, which might favor widespread genetic connectivity and ecological resilience unless physical dispersal barriers are present.
more »
« less
Genetic Variation in the Atlantic Bobtail Squid‐ Vibrio Symbiosis From the Galician Rías
ABSTRACT Symbiotic marine bacteria that are transmitted through the environment are susceptible to abiotic factors (salinity, temperature, physical barriers) that can influence their ability to colonize their specific hosts. Given that many symbioses are driven by host specificity, environmentally transmitted symbionts are more susceptible to extrinsic factors depending on conditions over space and time. In order to determine whether the population structure of environmentally transmitted symbionts reflects host specificity or biogeography, we analysed the genetic structure ofSepiola atlantica(Cephalopoda: Sepiolidae) and theirVibriosymbionts (V. fischeriandV. logei) in four Galician Rías (Spain). This geographical location is characterized by a jagged coastline with a deep‐sea entrance into the land, ideal for testing whether such population barriers exist due to genetic isolation. We used haplotype estimates combined with nested clade analysis to determine the genetic relatedness for bothS. atlanticaandVibriobacteria. Analyses of molecular variance (AMOVA) were used to estimate variation within and between populations for both host and symbiont genetic data. Our analyses reveal a low percentage of variation among and between host populations, suggesting that these populations are panmictic. In contrast,Vibriosymbiont populations show certain degree of genetic structure, demonstrating that the hydrology of the rías is driving bacterial distribution (and not host specificity). Thus, for environmentally transmitted symbioses such as the sepiolid squid‐Vibrioassociation, abiotic factors can be a major selective force for determining population structure for one of the partners.
more »
« less
- Award ID(s):
- 2214038
- PAR ID:
- 10594366
- Editor(s):
- King, K
- Publisher / Repository:
- Wiley
- Date Published:
- Journal Name:
- Molecular Ecology
- Volume:
- 34
- Issue:
- 1
- ISSN:
- 0962-1083
- Page Range / eLocation ID:
- e17596
- Subject(s) / Keyword(s):
- Vibrio sepiolid squid phylogeography Galicia
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract Background Marine symbioses are predominantly established through horizontal acquisition of microbial symbionts from the environment. However, genetic and functional comparisons of free-living populations of symbionts to their host-associated counterparts are sparse. Here, we assembled the first genomes of the chemoautotrophic gammaproteobacterial symbionts affiliated with the deep-sea snail Alviniconcha hessleri from two separate hydrothermal vent fields of the Mariana Back-Arc Basin. We used phylogenomic and population genomic methods to assess sequence and gene content variation between free-living and host-associated symbionts. Results Our phylogenomic analyses show that the free-living and host-associated symbionts of A. hessleri from both vent fields are populations of monophyletic strains from a single species. Furthermore, genetic structure and gene content analyses indicate that these symbiont populations are differentiated by vent field rather than by lifestyle. Conclusion Together, this work suggests that, despite the potential influence of host-mediated acquisition and release processes on horizontally transmitted symbionts, geographic isolation and/or adaptation to local habitat conditions are important determinants of symbiont population structure and intra-host composition.more » « less
-
Stochastic Fluctuations of the Facultative Endosymbiont Wolbachia due to Finite Host Population SizeABSTRACT Many insects and other animals host heritable endosymbionts that alter host fitness and reproduction. The prevalence of facultative endosymbionts can fluctuate in host populations across time and geography for reasons that are poorly understood. This is particularly true for maternally transmittedWolbachiabacteria, which infect roughly half of all insect species. For instance, the frequencies of severalwMel‐likeWolbachia, includingwMel in hostDrosophila melanogaster, fluctuate over time in certain host populations, but the specific conditions that generate temporal variation inWolbachiaprevalence are unresolved. We implemented a discrete generation model in the new R packagesymbiontmodelerto evaluate how finite‐population stochasticity contributes toWolbachiafluctuations over time in simulated host populations under a variety of conditions. Using empirical estimates from naturalWolbachia‐Drosophilasystems, we explored how stochasticity is determined by a broad range of factors, including host population size, maternal transmission rates, andWolbachiaeffects on host fitness (modeled as fecundity) and reproduction (cytoplasmic incompatibility; CI). While stochasticity generally increases when host fitness benefits and CI are relaxed, we found that a decline in the maternal transmission rate had the strongest relative impact on increasing the size of fluctuations. We infer that non‐ or weak‐CI‐causing strains likewMel, which often show evidence of imperfect maternal transmission, tend to generate larger stochastic fluctuations compared to strains that cause strong CI, likewRi inD. simulans. Additional factors, such as fluctuating host fitness effects, are required to explain the largest examples of temporal variation inWolbachia. The conditions we simulate here usingsymbiontmodelerserve as a jumping‐off point for understanding drivers of temporal and spatial variation in the prevalence ofWolbachia, the most common endosymbionts found in nature.more » « less
-
ABSTRACT In integrative distributional, demographic and coalescent (iDDC) modelling, a critical component is the statistical relationship between habitat suitability and local population sizes. This study explores this relationship in twoEnyaliuslizard species from the Brazilian Atlantic Forest: the high‐elevationE. iheringiiand low‐elevationE. catenatusand how this transformation affects spatiotemporal demographic inference. Most previous iDDC studies assumed a linear relationship, but this study hypothesises that the relationship may be nonlinear, especially for high‐elevation species with broader environmental tolerances. We test two key hypotheses: (1) The habitat suitability to population size relationship is nonlinear forE. iheringii(high‐elevation) and linear forE. catenatus(low‐elevation); and (2)E. iheringiiexhibits higher effective migration across populations thanE. catenatus. Our findings provide clear support for hypothesis (2), but mixed support for hypothesis (1), with strong model support for a nonlinear transformation in the high‐elevationE. iheringiiand some (albeit weak) support for a nonlinear transformation also inE. catenatus. The iDDC models allow us to generate landscape‐wide maps of predicted genetic diversity for both species, revealing that genetic diversity predictions for the high‐elevationE. iheringiialign with estimated patterns of historical range stability, whereas predictions for low‐elevationE. catenatusare distinct from range‐wide stability predictions. This research highlights the importance of accurately modelling the habitat suitability to population size relationship in iDDC studies, contributing to our understanding of species' demographic responses to environmental changes.more » « less
-
ABSTRACT Herbicide resistance in agricultural weeds has become one of the greatest challenges for sustainable crop production. The repeated evolution of herbicide resistance provides an excellent opportunity to study the genetic and physiological basis of the resistance phenotype and the evolutionary responses to human‐mediated selection pressures.Lolium multiflorumis a ubiquitous weed that has evolved herbicide resistance repeatedly around the world in various cropping systems. We assembled and annotated a chromosome‐scale genome forL. multiflorumand elucidated the genetic architecture of paraquat resistance by performing quantitative trait locus analysis, genome‐wide association studies, genetic divergence analysis and transcriptome analyses from paraquat‐resistant and ‐susceptibleL. multiflorumplants. We identified two regions on chromosome 5 that were associated with paraquat resistance. These regions both showed evidence for positive selection among the resistant populations we sampled, but the effects of this selection on the genome differed, implying a complex evolutionary history. In addition, these regions contained candidate genes that encoded cellular transport functions, including a novel multidrug and toxin extrusion (MATE) protein and a cation transporter previously shown to interact with polyamines. Given thatL. multiflorumis a weed and a cultivated crop species, the genomic resources generated will prove valuable to a wide spectrum of the plant science community. Our work contributes to a growing body of knowledge on the underlying evolutionary and ecological dynamics of rapid adaptation to strong anthropogenic selection pressure that could help initiate efforts to improve weed management practices in the long term for a more sustainable agriculture.more » « less
An official website of the United States government

