Suboptimal environmental conditions prolong phage epidemics in bacterial populations.

Infections by filamentous phages, which are usually nonlethal to the bacterial cells, influence bacterial fitness in various ways. While phage-encoded accessory genes, for example virulence genes, can be highly beneficial, the production of viral particles is energetically costly and often reduces bacterial growth. Consequently, if costs outweigh benefits, bacteria evolve resistance, which can shorten phage epidemics. Abiotic conditions are known to influence the net-fitness effect for infected bacteria. Their impact on the dynamics and trajectories of host resistance evolution, however, remains yet unknown. To address this, we experimentally evolved the bacterium Vibrio alginolyticus in the presence of a filamentous phage at three different salinity levels, that is (1) ambient, (2) 50% reduction and (3) fluctuations between reduced and ambient. In all three salinities, bacteria rapidly acquired resistance through super infection exclusion (SIE), whereby phage-infected cells acquired immunity at the cost of reduced growth. Over time, SIE was gradually replaced by evolutionary fitter surface receptor mutants (SRM). This replacement was significantly faster at ambient and fluctuating conditions compared with the low saline environment. Our experimentally parameterized mathematical model explains that suboptimal environmental conditions, in which bacterial growth is slower, slow down phage resistance evolution ultimately prolonging phage epidemics. Our results may explain the high prevalence of filamentous phages in natural environments where bacteria are frequently exposed to suboptimal conditions and constantly shifting selections regimes. Thus, our future ocean may favour the emergence of phage-born pathogenic bacteria and impose a greater risk for disease outbreaks, impacting not only marine animals but also humans.

Higher phage virulence accelerates the evolution of host resistance.

Pathogens vary strikingly in their virulence and the selection they impose on their hosts. While the evolution of different virulence levels is well studied, the evolution of host resistance in response to different virulence levels is less understood and, at present, mainly based on observations and theoretical predictions with few experimental tests. Increased virulence can increase selection for host resistance evolution if the benefits of avoiding infection outweigh resistance costs. To test this, we experimentally evolved the bacterium Vibrio alginolyticus in the presence of two variants of a filamentous phage that differ in their virulence. The bacterial host exhibited two alternative defence strategies: (1) super infection exclusion (SIE), whereby phage-infected cells were immune to subsequent infection at the cost of reduced growth, and (2) surface receptor mutations (SRM), providing resistance to infection by preventing phage attachment. While SIE emerged rapidly against both phages, SRM evolved faster against the high- than the low-virulence phage. Using a mathematical model of our system, we show that increasing virulence strengthens selection for SRM owing to the higher costs of infection suffered by SIE immune hosts. Thus, by accelerating the evolution of host resistance, more virulent phages caused shorter epidemics.

Gene expression remodelling and immune response during adaptive divergence in an African cichlid fish.

Variation in gene expression contributes to ecological speciation by facilitating population persistence in novel environments. Likewise, immune responses can be of relevance in speciation driven by adaptation to different environments. Previous studies examining gene expression differences between recently diverged ecotypes have often relied on only one pair of populations, targeted the expression of only a subset of genes or used wild-caught individuals. Here, we investigated the contribution of habitat-specific parasites and symbionts and the underlying immunological abilities of ecotype hosts to adaptive divergence in lake-river population pairs of the cichlid fish Astatotilapia burtoni. To shed light on the role of phenotypic plasticity in adaptive divergence, we compared parasite and microbiota communities, immune response, and gene expression patterns of fish from natural habitats and a lake-like pond set-up. In all investigated population pairs, lake fish were more heavily parasitized than river fish, in terms of both parasite taxon composition and infection abundance. The innate immune response in the wild was higher in lake than in river populations and was elevated in a river population exposed to lake parasites in the pond set-up. Environmental differences between lake and river habitat and their distinct parasite communities have shaped differential gene expression, involving genes functioning in osmoregulation and immune response. Most changes in gene expression between lake and river samples in the wild and in the pond set-up were based on a plastic response. Finally, gene expression and bacterial communities of wild-caught individuals and individuals acclimatized to lake-like pond conditions showed shifts underlying adaptive phenotypic plasticity.

Evolution of Polyploidy and Functional Diploidization in Sturgeons: Microsatellite Analysis in 10 Sturgeon Species.

Sturgeons (family Acipenseridae) are one of the most endangered groups of animals. Two hundred million years of evolution and multiple ploidy levels make this group a unique subject for studying the evolution of polyploidy in animals. As most sturgeon species have gone through significant functional diploidization, 2 scales of ploidy levels can be distinguished: the "evolutionary scale," which indicates the maximum ploidy level achieved and the "recent scale," which indicates the current functional ploidy level. This study analyzes published and new microsatellites to check the ploidy level and to determine the degrees of functional diploidization in 10 sturgeon species from Europe and Asia. We screened 50 primer pairs newly developed for Acipenser gueldenstaedtii and 40 primer pairs previously developed in other studies for other sturgeon species. The maximal number of alleles per individual of a given species was assessed at 20 microsatellite loci, which showed consistent amplification in most of the 10 analyzed species. Taken together, our data on the percentage of disomic loci in different species suggest that functional diploidization is an ongoing process in sturgeons. We observed lower levels of diploidization in tetraploid species from the Atlantic clade than in the species from the Pacific clade, which can be explained by the more recent genome duplication in tetraploid species from the Atlantic clade. Based on the recent findings and results of this study, we propose that the evolution of sturgeons has been affected by at least 3 different polyploidization events.

The effects of primary and secondary bacterial exposure on the seahorse (Hippocampus erectus) immune response.

Evolutionary adaptations in the Syngnathidae teleost family (seahorses, pipefish and seadragons) culminated in an array of spectacular morphologies, key immune gene losses, and the enigmatic male pregnancy. In seahorses, genome modifications associated with immunoglobulins, complement, and major histocompatibility complex (MHC II) pathway components raise questions concerning their immunological efficiency and the evolution of compensatory measures that may act in their place. In this investigation heat-killed bacteria (Vibrio aestuarianus and Tenacibaculum maritimum) were used in a two-phased experiment to assess the immune response dynamics of Hippocampus erectus. Gill transcriptomes from double and single-exposed individuals were analysed in order to determine the differentially expressed genes contributing to immune system responses towards immune priming. Double-exposed individuals exhibited a greater adaptive immune response when compared with single-exposed individuals, while single-exposed individuals, particularly with V. aestuarianus replicates, associated more with the innate branch of the immune system. T. maritimum double-exposed replicates exhibited the strongest immune reaction, likely due to their immunological naivety towards the bacterium, while there are also potential signs of innate trained immunity. MHC II upregulated expression was identified in selected V. aestuarianus-exposed seahorses, in the absence of other pathway constituents suggesting a possible alternative or non-classical MHC II immune function in seahorses. Gene Ontology (GO) enrichment analysis highlighted prominent angiogenesis activity following secondary exposure, which could be linked to an adaptive immune process in seahorses. This investigation highlights the prominent role of T-cell mediated adaptive immune responses in seahorses when exposed to sequential foreign bacteria exposures. If classical MHC II pathway function has been lost, innate trained immunity in syngnathids could be a potential compensatory mechanism.

Speciation dynamics and extent of parallel evolution along a lake-stream environmental contrast in African cichlid fishes.

Understanding the dynamics of speciation is a central topic in evolutionary biology. Here, we investigated how morphological and genomic differentiation accumulated along the speciation continuum in the African cichlid fish Astatotilapia burtoni. While morphological differentiation was continuously distributed across different lake-stream population pairs, we found that there were two categories with respect to genomic differentiation, suggesting a "gray zone" of speciation at ~0.1% net nucleotide divergence. Genomic differentiation was increased in the presence of divergent selection and drift compared to drift alone. The quantification of phenotypic and genetic parallelism in four cichlid species occurring along a lake-stream environmental contrast revealed parallel and antiparallel components in rapid adaptive divergence, and morphological convergence in species replicates inhabiting the same environments. Furthermore, we show that the extent of parallelism was higher when ancestral populations were more similar. Our study highlights the complementary roles of divergent selection and drift on speciation and parallel evolution.

Digest: Lab versus nature: Disease resistance evolution differs between environments.

Does disease resistance evolution in vitro reflect resistance evolution in vivo? Hernandez and Koskella conducted serial passage experiments of the plant pathogenic bacterium Pseudomonas syringae and two lytic bacteriophages in high-nutrient medium (in vitro) and in a tomato plant (in vivo). High levels of bacterial resistance to phages evolved in vitro but not in vivo, suggesting that high costs and low benefits of resistance explain the observed pattern.

Repeated Evolution Versus Common Ancestry: Sex Chromosome Evolution in the Haplochromine Cichlid Pseudocrenilabrus philander.

Why sex chromosomes turn over and remain undifferentiated in some taxa, whereas they degenerate in others, is still an area of ongoing research. The recurrent occurrence of homologous and homomorphic sex chromosomes in distantly related taxa suggests their independent evolution or continued recombination since their first emergence. Fishes display a great diversity of sex-determining systems. Here, we focus on sex chromosome evolution in haplochromines, the most species-rich lineage of cichlid fishes. We investigate sex-specific signatures in the Pseudocrenilabrus philander species complex, which belongs to a haplochromine genus found in many river systems and ichthyogeographic regions in northern, eastern, central, and southern Africa. Using whole-genome sequencing and population genetic, phylogenetic, and read-coverage analyses, we show that one population of P. philander has an XX-XY sex-determining system on LG7 with a large region of suppressed recombination. However, in a second bottlenecked population, we did not find any sign of a sex chromosome. Interestingly, LG7 also carries an XX-XY system in the phylogenetically more derived Lake Malawi haplochromine cichlids. Although the genomic regions determining sex are the same in Lake Malawi cichlids and P. philander, we did not find evidence for shared ancestry, suggesting that LG7 evolved as sex chromosome at least twice in haplochromine cichlids. Hence, our work provides further evidence for the labile nature of sex determination in fishes and supports the hypothesis that the same genomic regions can repeatedly and rapidly be recruited as sex chromosomes in more distantly related lineages.

Adaptive phenotypic plasticity contributes to divergence between lake and river populations of an East African cichlid fish.

Adaptive phenotypic plasticity and fixed genotypic differences have long been considered opposing strategies in adaptation. More recently, these mechanisms have been proposed to act complementarily and under certain conditions jointly facilitate evolution, speciation, and even adaptive radiations. Here, we investigate the relative contributions of adaptive phenotypic plasticity vs. local adaptation to fitness, using an emerging model system to study early phases of adaptive divergence, the generalist cichlid fish species Astatotilapia burtoni. We tested direct fitness consequences of morphological divergence between lake and river populations in nature by performing two transplant experiments in Lake Tanganyika. In the first experiment, we used wild-caught juvenile lake and river individuals, while in the second experiment, we used F1 crosses between lake and river fish bred in a common garden setup. By tracking the survival and growth of translocated individuals in enclosures in the lake over several weeks, we revealed local adaptation evidenced by faster growth of the wild-caught resident population in the first experiment. On the other hand, we did not find difference in growth between different types of F1 crosses in the second experiment, suggesting a substantial contribution of adaptive phenotypic plasticity to increased immigrant fitness. Our findings highlight the value of formally comparing fitness of wild-caught and common garden-reared individuals and emphasize the necessity of considering adaptive phenotypic plasticity in the study of adaptive divergence.

Immigrant and extrinsic hybrid inviability contribute to reproductive isolation between lake and river cichlid ecotypes.

Understanding how reproductive barriers evolve and which barriers contribute to speciation requires the examination of organismal lineages that are still in the process of diversification and the study of the full range of reproductive barriers acting at different life stages. Lake and river ecotypes of the East African cichlid fish Astatotilapia burtoni show habitat-specific adaptations, despite different levels of genetic differentiation, and thus represent an ideal model to study the evolution of reproductive barriers. To evaluate the degree of reproductive isolation between genetically divergent lake and river populations, we performed a mesocosm mating experiment in a semi-natural setting at Lake Tanganyika. We assessed reproductive isolation in the presence of male-male competition by analyzing survival and growth rates of introduced adults and their reproductive success from genetic parentage of surviving offspring. The genetically divergent river population showed reduced fitness in terms of survival, growth rate, and mating success in a lake-like environment. Hybrid offspring between different populations showed intermediate survival consistent with extrinsic postzygotic reproductive barriers. Our results suggest that both prezygotic (immigrant inviability) and postzygotic reproductive barriers contribute to divergence, and highlight the value of assessing multiple reproductive barriers acting at different stages and in natural contexts to understand speciation mechanisms.