The effect of immigration on the adaptation of microbial communities to warming

Theory predicts that immigration can either enhance or impair the rate at which species and whole communities adapt to environmental change, depending on the traits of genotypes and species in the source pool relative to local conditions. These responses in turn will determine how well whole communities function in changing environments. We tested the effects of immigration and experimental warming on microbial communities during an 81 day field experiment. The effects of immigration depended on the warming treatment. In warmed communities immigration was detrimental to community growth whereas in ambient communities it was beneficial. This result is explained if colonists came from a local species pool pre-adapted to ambient conditions. Loss of metabolic diversity, however, was buffered by immigration in both environments. Communities showed increasing local adaptation to temperature conditions during the experiment and this was independent of whether or not they received immigration. Genotypes that comprised the communities were not locally adapted, however, indicating that community local adaptation can be independent of adaptation of component genotypes. Our results are consistent with a greater role for species interactions rather than adaptation of constituent species in determining local adaptation of whole communities, and confirm that immigration can either enhance or impair community responses to environmental change depending on the environmental context

A rapid and scalable method for multilocus species delimitation using Bayesian model comparison and rooted triplets

Multilocus sequence data provide far greater power to resolve species limits than the single locus data typically used for broad surveys of clades. However, current statistical methods based on a multispecies coalescent framework are computationally demanding, because of the number of possible delimitations that must be compared and time-consuming likelihood calculations. New methods are therefore needed to open up the power of multilocus approaches to larger systematic surveys. Here, we present a rapid and scalable method that introduces two new innovations. First, the method reduces the complexity of likelihood calculations by decomposing the tree into rooted triplets. The distribution of topologies for a triplet across multiple loci has a uniform trinomial distribution when the 3 individuals belong to the same species, but a skewed distribution if they belong to separate species with a form that is specified by the multispecies coalescent. A Bayesian model comparison framework was developed and the best delimitation found by comparing the product of posterior probabilities of all triplets. The second innovation is a new dynamic programming algorithm for finding the optimum delimitation from all those compatible with a guide tree by successively analyzing subtrees defined by each node. This algorithm removes the need for heuristic searches used by current methods, and guarantees that the best solution is found and potentially could be used in other systematic applications. We assessed the performance of the method with simulated, published and newly generated data. Analyses of simulated data demonstrate that the combined method has favourable statistical properties and scalability with increasing sample sizes. Analyses of empirical data from both eukaryotes and prokaryotes demonstrate its potential for delimiting species in real cases

Effects of phylogenetic reconstruction method on the robustness of species delimitation using single-locus data

1. Coalescent-based species delimitation methods combine population genetic and phylogenetic theory to provide an objective means for delineating evolutionarily significant units of diversity. The Generalized Mixed Yule Coalescent (GMYC) and the Poisson Tree Process (PTP) are methods that use ultrametric (GMYC or PTP) or non-ultrametric (PTP) gene trees as input, intended for use mostly with single-locus data such as DNA barcodes. 2. Here we assess how robust the GMYC and PTP are to different phylogenetic reconstruction and branch smoothing methods. We reconstruct over 400 ultrametric trees using up to 30 different combinations of phylogenetic and smoothing methods and perform over 2,000 separate species delimitation analyses across 16 empirical datasets. We then assess how variable diversity estimates are, in terms of richness and identity, with respect to species delimitation, phylogenetic and smoothing methods. 3. The PTP method generally generates diversity estimates that are more robust to different phylogenetic methods. The GMYC is more sensitive, but provides consistent estimates for BEAST trees. The lower consistency of GMYC estimates is likely a result of differences among gene trees introduced by the smoothing step. Unresolved nodes (real anomalies or methodological artefacts) affect both GMYC and PTP estimates, but have a greater effect on GMYC estimates. Branch smoothing is a difficult step and perhaps an underappreciated source of bias that may be widespread among studies of diversity and diversification. 4. Nevertheless, careful choice of phylogenetic method does produce equivalent PTP and GMYC diversity estimates. We recommend simultaneous use of the PTP model with any model-based gene tree (e.g. RAxML) and GMYC approaches with BEAST trees for obtaining species hypotheses

Sexual species are separated by larger genetic gaps than asexual species in rotifers.

Why organisms diversify into discrete species instead of showing a continuum of genotypic and phenotypic forms is an important yet rarely studied question in speciation biology. Does species discreteness come from adaptation to fill discrete niches or from interspecific gaps generated by reproductive isolation? We investigate the importance of reproductive isolation by comparing genetic discreteness, in terms of intra- and interspecific variation, between facultatively sexual monogonont rotifers and obligately asexual bdelloid rotifers. We calculated the age (phylogenetic distance) and average pairwise genetic distance (raw distance) within and among evolutionarily significant units of diversity in six bdelloid clades and seven monogonont clades sampled for 4211 individuals in total. We find that monogonont species are more discrete than bdelloid species with respect to divergence between species but exhibit similar levels of intraspecific variation (species cohesiveness). This pattern arises because bdelloids have diversified into discrete genetic clusters at a faster net rate than monogononts. Although sampling biases or differences in ecology that are independent of sexuality might also affect these patterns, the results are consistent with the hypothesis that bdelloids diversified at a faster rate into less discrete species because their diversification does not depend on the evolution of reproductive isolation

Horizontal gene transfer in bdelloid rotifers is ancient, ongoing and more frequent in species from desiccating habitats.

BACKGROUND: Although prevalent in prokaryotes, horizontal gene transfer (HGT) is rarer in multicellular eukaryotes. Bdelloid rotifers are microscopic animals that contain a higher proportion of horizontally transferred, non-metazoan genes in their genomes than typical of animals. It has been hypothesized that bdelloids incorporate foreign DNA when they repair their chromosomes following double-strand breaks caused by desiccation. HGT might thereby contribute to species divergence and adaptation, as in prokaryotes. If so, we expect that species should differ in their complement of foreign genes, rather than sharing the same set of foreign genes inherited from a common ancestor. Furthermore, there should be more foreign genes in species that desiccate more frequently. We tested these hypotheses by surveying HGT in four congeneric species of bdelloids from different habitats: two from permanent aquatic habitats and two from temporary aquatic habitats that desiccate regularly. RESULTS: Transcriptomes of all four species contain many genes with a closer match to non-metazoan genes than to metazoan genes. Whole genome sequencing of one species confirmed the presence of these foreign genes in the genome. Nearly half of foreign genes are shared between all four species and an outgroup from another family, but many hundreds are unique to particular species, which indicates that HGT is ongoing. Using a dated phylogeny, we estimate an average of 12.8 gains versus 2.0 losses of foreign genes per million years. Consistent with the desiccation hypothesis, the level of HGT is higher in the species that experience regular desiccation events than those that do not. However, HGT still contributed hundreds of foreign genes to the species from permanently aquatic habitats. Foreign genes were mainly enzymes with various annotated functions that include catabolism of complex polysaccharides and stress responses. We found evidence of differential loss of ancestral foreign genes previously associated with desiccation protection in the two non-desiccating species. CONCLUSIONS: Nearly half of foreign genes were acquired before the divergence of bdelloid families over 60 Mya. Nonetheless, HGT is ongoing in bdelloids and has contributed to putative functional differences among species. Variation among our study species is consistent with the hypothesis that desiccating habitats promote HGT

Detecting evolutionarily significant units above the species level using the generalised mixed Yule coalescent method

1. There is renewed interest in inferring evolutionary history by modelling diversification rates using phylogenies. Understanding the performance of the methods used under different scenarios is essential for assessing empirical results. Recently, we introduced a new approach for analysing broadscale diversity patterns, using the generalised mixed Yule coalescent (GMYC) method to test for the existence of evolutionarily significant units above the species (higher ESUs). This approach focuses on identifying clades as well as estimating rates, and we refer to it as clade-dependent. However, the ability of the GMYC to detect the phylogenetic signature of higher ESUs has not been fully explored, nor has it been placed in the context of other, clade-independent approaches. 2. We simulated >32 000 trees under two clade-independent models: constant-rate birth-death (CRBD) and variable-rate birth-death (VRBD), using parameter estimates from nine empirical trees and more general parameter values. The simulated trees were used to evaluate scenarios under which GMYC might incorrectly detect the presence of higher ESUs. 3. The GMYC null model was rejected at a high rate on CRBD-simulated trees. This would lead to spurious inference of higher ESUs. However, the support for the GMYC model was significantly greater in most of the empirical clades than expected under a CRBD process. Simulations with empirically derived parameter values could therefore be used to exclude CRBD as an explanation for diversification patterns. In contrast, a VRBD process could not be ruled out as an alternative explanation for the apparent signature of hESUs in the empirical clades, based on the GMYC method alone. Other metrics of tree shape, however, differed notably between the empirical and VRBD-simulated trees. These metrics could be used in future to distinguish clade-dependent and clade-independent models. 4. In conclusion, detection of higher ESUs using the GMYC is robust against some clade-independent models, as long as simulations are used to evaluate these alternatives, but not against others. The differences between clade-dependent and clade-independent processes are biologically interesting, but most current models focus on the latter. We advocate more research into clade-dependent models for broad diversity patterns

Author Correction : Bacterial adaptation is constrained in complex communities (Nature Communications, (2020), 11, 1, (754), 10.1038/s41467-020-14570-z)

The original version of this Article contained an error in Fig. 1, in which the labels were inadvertently omitted from the pie chart. This has been corrected in both the PDF and HTML versions of the Article

Soil aggregates as massively concurrent evolutionary incubators

Soil aggregation, a key component of soil structure, has mostly been examined from the perspective of soil management and the mediation of ecosystem processes such as soil carbon storage. However, soil aggregation is also a major factor to consider in terms of the fine-scale organization of the soil microbiome. For example, the physico-chemical conditions inside of aggregates usually differ from the conditions prevalent in the bulk soil and aggregates therefore increase the spatial heterogeneity of the soil. In addition, aggregates can provide a refuge for microbes against predation since their interior is not accessible to many predators. Soil aggregates are thus clearly important for microbial community ecology in soils (for example, Vos et al., 2013; Rillig et al., 2016) and for microbially driven biogeochemistry, and soil microbial ecologists are increasingly appreciating these aspects of soil aggregation. Soil aggregates have, however, so far been neglected when it comes to evolutionary considerations (Crawford et al., 2005) and we here propose that the process of soil aggregation should be considered as an important driver of evolution in the soil microbial community