Long-term gut microbiome dynamics in Drosophila melanogaster reveal environment-specific associations between bacterial taxa at the family level.

The influence of the microbiome on its host is well-documented, but the interplay of its members is not yet well-understood. Even for simple microbiomes, the interaction among members of the microbiome is difficult to study. Longitudinal studies provide a promising approach to studying such interactions through the temporal covariation of different taxonomic units. By contrast to most longitudinal studies, which span only a single host generation, we here present a post hoc analysis of a whole-genome dataset of 81 samples that follows microbiome composition for up to 180 host generations, which cover nearly 10 years. The microbiome diversity remained rather stable in replicated Drosophila melanogaster populations exposed to two different temperature regimes. The composition changed, however, systematically across replicates of the two temperature regimes. Significant associations between families, mostly specific to one temperature regime, indicate functional interdependence of different microbiome components. These associations also involve moderately abundant families, which emphasizes their functional importance, and highlights the importance of looking beyond the common constituents of the Drosophila microbiome.

Long-Term Dynamics Among Wolbachia Strains During Thermal Adaptation of Their Drosophila melanogaster Hosts.

Climate change is a major evolutionary force triggering thermal adaptation in a broad range of species. While the consequences of global warming are being studied for an increasing number of species, limited attention has been given to the evolutionary dynamics of endosymbionts in response to climate change. Here, we address this question by studying the dynamics of Wolbachia, a well-studied endosymbiont of Drosophila melanogaster. D. melanogaster populations infected with 13 different Wolbachia strains were exposed to novel hot and cold laboratory environments for up to 180 generations. The short-term dynamics suggested a temperature-related fitness difference resulting in the increase of clade V strains in the cold environment only. Our long-term analysis now uncovers that clade V dominates in all replicates after generation 60 irrespective of temperature treatment. We propose that adaptation of the Drosophila host to either temperature or Drosophila C virus (DCV) infection are the cause of the replicated, temporally non-concordant Wolbachia dynamics. Our study provides an interesting case demonstrating that even simple, well-controlled experiments can result in complex, but repeatable evolutionary dynamics, thus providing a cautionary note on too simple interpretations on the impact of climate change.

DNA Motifs Are Not General Predictors of Recombination in Two Drosophila Sister Species.

Meiotic recombination is crucial for chromosomal segregation and facilitates the spread of beneficial and removal of deleterious mutations. Recombination rates frequently vary along chromosomes and Drosophila melanogaster exhibits a remarkable pattern. Recombination rates gradually decrease toward centromeres and telomeres, with a dramatic impact on levels of variation in natural populations. Two close sister species, Drosophila simulans and Drosophila mauritiana do not only have higher recombination rates but also exhibit a much more homogeneous recombination rate that only drops sharply very close to centromeres and telomeres. Because certain sequence motifs are associated with recombination rate variation in D. melanogaster, we tested whether the difference in recombination landscape between D. melanogaster and D. simulans can be explained by the genomic distribution of recombination rate-associated sequence motifs. We constructed the first high-resolution recombination map for D. simulans based on 189 haplotypes from a natural D. simulans population and searched for short sequence motifs linked with higher than average recombination in both sister species. We identified five consensus motifs significantly associated with higher than average chromosome-wide recombination rates in at least one species and present in both. Testing fine resolution associations between motif density and recombination, we found strong and positive associations genome-wide over a range of scales in D. melanogaster, while the results were equivocal in D. simulans. Despite the strong association in D. melanogaster, we did not find a decreasing density of these short-repeat motifs toward centromeres and telomeres. We conclude that the density of recombination-associated repeat motifs cannot explain the large-scale recombination landscape in D. melanogaster, nor the differences to D. simulans. The strong association seen for the sequence motifs in D. melanogaster likely reflects their impact influencing local differences in recombination rates along the genome.

Epidemiological, evolutionary, and economic determinants of eradication tails.

Despite modern medical interventions, infectious diseases continue to generate huge socio-economic losses. The benefits of eradicating a disease are therefore high. While successful with smallpox and rinderpest, many other eradication attempts have failed. Eradications require huge and costly efforts, which can be sustained only if sufficient progress can be achieved. While initial successes are usually obtained more easily, progress often becomes harder as a disease becomes rare in the eradication endgame. A long eradication tail of slowly decreasing incidence levels can frustrate eradication efforts, as it becomes unclear whether progress toward eradication is still being made and how much more needs to be invested to push the targeted disease beyond its extinction threshold. Realistic disease dynamics are complicated by evolutionary responses to interventions and by interactions among different temporal and spatial scales. Models accounting for these complexities are required for understanding the shapes of eradication tails. In particular, such models allow predicting how hard or costly eradication will be, and may even inform in which manner progress has to be assessed during the eradication endgame. Here we outline a general procedure by analyzing the eradication tails of generic SIS diseases, taking into account two major ingredients of realistic complexity: a group-structured host population in which host contacts within groups are more likely than host contacts between groups, and virulence evolution subject to a trade-off between host infectivity within groups and host mobility among groups. Disentangling the epidemiological, evolutionary, and economic determinants of eradication tails, we show how tails of different shapes arise depending on salient model parameters and on how the extinction threshold is approached. We find that disease evolution generally extends the eradication tail and show how the cost structure of eradication measures plays a key role in shaping eradication tails.

Evolutionary branching in complex landscapes.

Divergent adaptation to different environments can promote speciation, and it is thus important to consider spatial structure in models of speciation. Earlier theoretical work, however, has been limited to particularly simple types of spatial structure (linear environmental gradients and spatially discrete metapopulations), leaving unaddressed the effects of more realistic patterns of landscape heterogeneity, such as nonlinear gradients and spatially continuous patchiness. To elucidate the consequences of such complex landscapes, we adapt an established spatially explicit individual-based model of evolutionary branching. We show that branching is most probable at intermediate levels of various types of heterogeneity and that different types of heterogeneity have, to some extent, additive effects in promoting branching. In contrast to such additivity, we find a novel refugium effect in which refugia in hostile environments provide opportunities for colonization, thus increasing the probability of branching in patchy landscapes. Effects of patchiness depend on the scale of patches relative to dispersal. Providing a needed connection to empirical research on biodiversity and conservation policy, we introduce empirically accessible spatial environmental metrics that quantitatively predict a landscape's branching propensity.

Abrupt community transitions and cyclic evolutionary dynamics in complex food webs.

Understanding the emergence and maintenance of biodiversity ranks among the most fundamental challenges in evolutionary ecology. While processes of community assembly have frequently been analyzed from an ecological perspective, their evolutionary dimensions have so far received less attention. To elucidate the eco-evolutionary processes underlying the long-term build-up and potential collapse of community diversity, here we develop and examine an individual-based model describing coevolutionary dynamics driven by trophic interactions and interference competition, of a pair of quantitative traits determining predator and prey niches. Our results demonstrate the (1) emergence of communities with multiple trophic levels, shown here for the first time for stochastic models with linear functional responses, and (2) intermittent and cyclic evolutionary transitions between two alternative community states. In particular, our results indicate that the interplay of ecological and evolutionary dynamics often results in extinction cascades that remove the entire trophic level of consumers from a community. Finally, we show the (3) robustness of our results under variations of model assumptions, underscoring that processes of consumer collapse and subsequent rebound could be important elements of understanding biodiversity dynamics in natural communities.

Sexual selection enables long-term coexistence despite ecological equivalence.

Empirical data indicate that sexual preferences are critical for maintaining species boundaries, yet theoretical work has suggested that, on their own, they can have only a minimal role in maintaining biodiversity. This is because long-term coexistence within overlapping ranges is thought to be unlikely in the absence of ecological differentiation. Here we challenge this widely held view by generalizing a standard model of sexual selection to include two ubiquitous features of populations with sexual selection: spatial variation in local carrying capacity, and mate-search costs in females. We show that, when these two features are combined, sexual preferences can single-handedly maintain coexistence, even when spatial variation in local carrying capacity is so slight that it might go unnoticed empirically. This theoretical study demonstrates that sexual selection alone can promote the long-term coexistence of ecologically equivalent species with overlapping ranges, and it thus provides a novel explanation for the maintenance of species diversity.

Invasion and persistence of infectious agents in fragmented host populations.

One of the important questions in understanding infectious diseases and their prevention and control is how infectious agents can invade and become endemic in a host population. A ubiquitous feature of natural populations is that they are spatially fragmented, resulting in relatively homogeneous local populations inhabiting patches connected by the migration of hosts. Such fragmented population structures are studied extensively with metapopulation models. Being able to define and calculate an indicator for the success of invasion and persistence of an infectious agent is essential for obtaining general qualitative insights into infection dynamics, for the comparison of prevention and control scenarios, and for quantitative insights into specific systems. For homogeneous populations, the basic reproduction ratio R(0) plays this role. For metapopulations, defining such an 'invasion indicator' is not straightforward. Some indicators have been defined for specific situations, e.g., the household reproduction number R*. However, these existing indicators often fail to account for host demography and especially host migration. Here we show how to calculate a more broadly applicable indicator R(m) for the invasion and persistence of infectious agents in a host metapopulation of equally connected patches, for a wide range of possible epidemiological models. A strong feature of our method is that it explicitly accounts for host demography and host migration. Using a simple compartmental system as an example, we illustrate how R(m) can be calculated and expressed in terms of the key determinants of epidemiological dynamics.

The evolution of conditional dispersal and reproductive isolation along environmental gradients.

Dispersal modulates gene flow throughout a population's spatial range. Gene flow affects adaptation at local spatial scales, and consequently impacts the evolution of reproductive isolation. A recent theoretical investigation has demonstrated that local adaptation along an environmental gradient, facilitated by the evolution of limited dispersal, can lead to parapatric speciation even in the absence of assortative mating. This and other studies assumed unconditional dispersal, so individuals start dispersing without regard to local environmental conditions. However, many species disperse conditionally; their propensity to disperse is contingent upon environmental cues, such as the degree of local crowding or the availability of suitable mates. Here, we use an individual-based model in continuous space to investigate by numerical simulation the relationship between the evolution of threshold-based conditional dispersal and parapatric speciation driven by frequency-dependent competition along environmental gradients. We find that, as with unconditional dispersal, parapatric speciation occurs under a broad range of conditions when reproduction is asexual, and under a more restricted range of conditions when reproduction is sexual. In both the asexual and sexual cases, the evolution of conditional dispersal is strongly influenced by the slope of the environmental gradient: shallow environmental gradients result in low dispersal thresholds and high dispersal distances, while steep environmental gradients result in high dispersal thresholds and low dispersal distances. The latter, however, remain higher than under unconditional dispersal, thus undermining isolation by distance, and hindering speciation in sexual populations. Consequently, the speciation of sexual populations under conditional dispersal is triggered by a steeper gradient than under unconditional dispersal. Enhancing the disruptiveness of frequency-dependent selection, more box-shaped competition kernels dramatically lower the speciation-enabling slope of the environmental gradient.