The gut microbiota is crucial for many aspects of their hosts’ biology, and it has been characterized for many species across the animal kingdom. Yet, we still don’t have a good understanding of ...whether non-lethal sampling can accurately capture the diversity of gut-associated bacterial communities, as estimated from lethal sampling of intestinal tissue. We further lack knowledge on whether non-lethal sampling methods are suitable for detecting gut microbiota shifts associated with changes in environmental factors (e.g., diet). We addressed these questions in threespine stickleback fish, a model system for evolutionary ecology, by comparing bacterial communities from intestinal tissue and feces. Despite some differences in community composition between the two sample types and considerable temporal variation among fecal samples, bacterial communities appear to largely overlap. Further, we detected consistent and significant changes of fecal bacterial communities associated with an experimental diet manipulation. This suggests that fecal sampling can represent an adequate non-lethal method to characterize the gut microbiota of threespine stickleback, but additional studies will be necessary before drawing general conclusions regarding the validity of fecal sampling for gut microbiota studies. To this end, we give recommendations to improve the characterization of the gut microbiota via fecal sampling. Fecal sampling allows studying temporal gut microbiota shifts associated with environmental change at the individual level, which increases opportunities for future experimental gut microbiota research.
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Background
The question of which ecological and evolutionary processes structure the distribution of biodiversity has intrigued scientists for centuries, and historically, inferences have been gained ...predominantly by studying animals and plants. Although substantial progress has been made towards understanding the multitude of factors that shape host‐associated microbial communities (i.e., microbiomes), it remains largely unknown whether large‐scale geographical patterns in diversity observed for macroorganisms also apply for their microbiomes and whether microbiomes are shaped by the same processes that appear key for determining biogeographical patterns in their hosts.
The geographical distribution of microbiome diversity
We discuss challenges and potential approaches for studying microbiome biogeography, with the goal of inspiring future lines of research that can stimulate the development of new ecological and evolutionary theory in the microbiome field. The theory and examples presented here focus specifically on bacterial microbiomes, and we give an overview of host‐associated bacterial microbiome research beginning to examine some of the classic biodiversity patterns central to the fields of ecology and evolution.
Potential impacts of microbiome variation for host ecology and evolution
Microbiome diversity patterns are particularly important to consider because microbes are crucial for many aspects of the biology of their hosts. We discuss how more comprehensive knowledge of the geographical variation of microbiome diversity at the host individual and population levels might be crucial for understanding host ecology and evolution.
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Organismal divergence can be driven by differential resource use and adaptation to different trophic niches. Variation in diet is a major factor shaping the gut microbiota, which is crucial for many ...aspects of their hosts’ biology. However, it remains largely unknown how host diet diversity affects the gut microbiota, and it could be hypothesized that trophic niche width is positively associated with gut microbiota diversity. To test this idea, we sequenced the 16S ribosomal RNA gene from intestinal tissue of 14 threespine stickleback populations from lakes of varying size on Vancouver Island, Canada, that have been shown to differ in trophic niche width. Using lake size as a proxy for trophic ecology, we found evidence for higher gut microbiota uniqueness among individuals from populations with broader trophic niches. While these results suggest that diet diversity might promote gut microbiota diversity, additional work investigating diet and gut microbiota variation of the same host organisms will be necessary. Yet our results motivate the question of how host population diversity (e.g., ecological, morphological, genetic) might interact with the gut microbiota during the adaptation to ecological niches.
Abstract Pigmentation is an excellent trait to examine patterns of evolutionary change because it is often under natural selection. Benthic and limnetic threespine stickleback ( Gasterosteus ...aculeatus ) exhibit distinct pigmentation phenotypes, likely an adaptation to occupation of divergent niches. The genetic architecture of pigmentation in vertebrates appears to be complex. Prior QTL mapping of threespine stickleback pigmentation phenotypes has identified several candidate loci. However—relative to other morphological phenotypes (e.g., spines or lateral plates)—the genetic architecture of threespine stickleback pigmentation remains understudied. Here, we performed QTL mapping for two melanic pigmentation traits (melanophore density and lateral barring) using benthic-limnetic F 2 crosses. The two traits mapped to different chromosomes, suggesting a distinct genetic basis. The resulting QTLs were additive, but explained a relatively small fraction of the total variance (~6%). QTLs maps differed by F 1 family, suggesting variation in genetic architecture or ability to detect loci of small effect. Functional analysis identified enriched pathways for candidate loci. Several of the resulting candidate loci for pigmentation, including three loci in enriched pathways ( bco1 , sulf1 , and tyms ) have been previously indicated to affect pigmentation in other vertebrates. These findings add to a growing body of evidence suggesting pigmentation is often polygenic.
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The processes of local adaptation and ecological speciation are often strongly shaped by biotic interactions such as competition and predation. One of the strongest lines of evidence that biotic ...interactions drive evolution comes from the repeated divergence of lineages in association with repeated changes in the community of interacting species. Yet relatively little is known about the repeatability of changes in gut microbial communities and their role in adaptation and divergence of host populations in nature. Here we use three cases of rapid, parallel adaptation and speciation in freshwater threespine stickleback to test for parallel changes in associated gut microbiomes. We find that features of the gut microbial communities have shifted repeatedly in the same direction in association with parallel divergence and speciation of stickleback hosts. These results suggest that changes to gut microbiomes can occur rapidly and predictably in conjunction with host evolution, and that host-microbe interactions might play an important role in host adaptation and diversification.
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Hybrid incompatibilities occur when interactions between opposite ancestry alleles at different loci reduce the fitness of hybrids. Most work on incompatibilities has focused on those that are ..."intrinsic," meaning they affect viability and sterility in the laboratory. Theory predicts that ecological selection can also underlie hybrid incompatibilities, but tests of this hypothesis using sequence data are scarce. In this article, we compiled genetic data for F2 hybrid crosses between divergent populations of threespine stickleback fish (Gasterosteus aculeatus L.) that were born and raised in either the field (seminatural experimental ponds) or the laboratory (aquaria). Because selection against incompatibilities results in elevated ancestry heterozygosity, we tested the prediction that ancestry heterozygosity will be higher in pond-raised fish compared to those raised in aquaria. We found that ancestry heterozygosity was elevated by approximately 3% in crosses raised in ponds compared to those raised in aquaria. Additional analyses support a phenotypic basis for incompatibility and suggest that environment-specific single-locus heterozygote advantage is not the cause of selection on ancestry heterozygosity. Our study provides evidence that, in stickleback, a coarse-albeit indirect-signal of environment-dependent hybrid incompatibility is reliably detectable and suggests that extrinsic incompatibilities can evolve before intrinsic incompatibilities.
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Policies ensuring that research data are available on public archives are increasingly being implemented at the government 1, funding agency 2–4, and journal 5, 6 level. These policies are predicated ...on the idea that authors are poor stewards of their data, particularly over the long term 7, and indeed many studies have found that authors are often unable or unwilling to share their data 8–11. However, there are no systematic estimates of how the availability of research data changes with time since publication. We therefore requested data sets from a relatively homogenous set of 516 articles published between 2 and 22 years ago, and found that availability of the data was strongly affected by article age. For papers where the authors gave the status of their data, the odds of a data set being extant fell by 17% per year. In addition, the odds that we could find a working e-mail address for the first, last, or corresponding author fell by 7% per year. Our results reinforce the notion that, in the long term, research data cannot be reliably preserved by individual researchers, and further demonstrate the urgent need for policies mandating data sharing via public archives.
•We examined the availability of data from 516 studies between 2 and 22 years old•The odds of a data set being reported as extant fell by 17% per year•Broken e-mails and obsolete storage devices were the main obstacles to data sharing•Policies mandating data archiving at publication are clearly needed
Vines et al. ask authors for the data underlying papers between 2 and 22 years old and find that the odds of it being reported extant decrease by 17% for every year since publication.
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(Non)Parallel Evolution Bolnick, Daniel I; Barrett, Rowan D.H; Oke, Krista B ...
Annual review of ecology, evolution, and systematics,
11/2018, Volume:
49, Issue:
1
Journal Article
Peer reviewed
Parallel evolution across replicate populations has provided evolutionary biologists with iconic examples of adaptation. When multiple populations colonize seemingly similar habitats, they may evolve ...similar genes, traits, or functions. Yet, replicated evolution in nature or in the laboratory often yields inconsistent outcomes: Some replicate populations evolve along highly similar trajectories, whereas other replicate populations evolve to different extents or in distinct directions. To understand these heterogeneous outcomes, biologists are increasingly treating parallel evolution not as a binary phenomenon but rather as a quantitative continuum ranging from parallel to nonparallel. By measuring replicate populations' positions along this (non)parallel continuum, we can test hypotheses about evolutionary and ecological factors that influence the extent of repeatable evolution. We review evidence regarding the manifestation of (non)parallel evolution in the laboratory, in natural populations, and in applied contexts such as cancer. We enumerate the many genetic, ecological, and evolutionary processes that contribute to variation in the extent of parallel evolution.
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Adaptation to new environments often occurs in the face of gene flow. Under these conditions, gene flow and recombination can impede adaptation by breaking down linkage disequilibrium between locally ...adapted alleles. Theory predicts that this decay can be halted or slowed if adaptive alleles are tightly linked in regions of low recombination, potentially favouring divergence and adaptive evolution in these regions over others. Here, we compiled a global genomic data set of over 1,300 individual threespine stickleback from 52 populations and compared the tendency for adaptive alleles to occur in regions of low recombination between populations that diverged with or without gene flow. In support of theory, we found that putatively adaptive alleles (FST and dXY outliers) tend to occur more often in regions of low recombination in populations where divergent selection and gene flow have jointly occurred. This result remained significant when we employed different genomic window sizes, controlled for the effects of mutation rate and gene density, controlled for overall genetic differentiation, varied the genetic map used to estimate recombination and used a continuous (rather than discrete) measure of geographic distance as proxy for gene flow/shared ancestry. We argue that our study provides the first statistical evidence that the interaction of gene flow and selection biases divergence toward regions of low recombination.
see also the Perspective by Marques
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Highly pleiotropic genes are predicted to be used less often during adaptation, as mutations in these loci are more likely to have negative fitness consequences. Following this logic, we tested ...whether pleiotropy impacts the probability that a locus will be used repeatedly in adaptation. We used two proxies to estimate pleiotropy: number of phenotypic traits affected by a given genomic region and gene connectivity. We first surveyed 16 independent stream‐lake and three independent benthic‐limnetic ecotype pairs of threespine stickleback to estimate genome‐wide patterns in parallel genomic differentiation. Our analysis revealed parallel divergence across the genome; 30%–37% of outlier regions were shared between at least two independent pairs in either the stream‐lake or benthic‐limnetic comparisons. We then tested whether parallel genomic regions are less pleiotropic than nonparallel regions. Counter to our a priori prediction, parallel genomic regions contained genes with significantly more pleiotropy; that is, influencing a greater number of traits and more highly connected. The increased pleiotropy of parallel regions could not be explained by other genomic factors, as there was no significant difference in mean gene count, mutation or recombination rates between parallel and nonparallel regions. Interestingly, although nonparallel regions contained genes that were less connected and influenced fewer mapped traits on average than parallel regions, they also tended to contain the genes that were predicted to be the most pleiotropic. Taken together, our findings are consistent with the idea that pleiotropy only becomes constraining at high levels and that low or intermediate levels of pleiotropy may be beneficial for adaptation.
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