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Agashe, D.

Publications and source records attributed to Agashe, D..

34 records · Page 2Linked to original sources

Evolutionary jumps in bacterial GC content

Genomic GC content is a fundamental molecular trait linked with many key genomic features such as codon and amino acid use. Across bacteria, GC content is surprisingly diverse and has been studied for many decades; yet its evolution remains incompletely understood. Since it is difficult to observe GC content evolve on laboratory time-scales, phylogenetic comparative approaches are instrumental; but this dimension is rarely studied systematically in the case of bacterial GC content. We applied phylogenetic comparative models to analyse GC content evolution in multiple bacterial groups across two major bacterial phyla. We find that GC content diversifies via a combination of gradual evolution and evolutionary "jumps". Surprisingly, unlike prior reports that solely focused on reductions in GC, we found a comparable number of jumps with both increased and decreased GC content. Overall, many of the identified jumps occur in lineages beyond the well-studied peculiar examples of endosymbiotic and AT-rich marine bacteria, and do not support the predicted role of oxygen dependence. Our analysis of rapid and large shifts in GC content thus identifies new clades and novel contexts to further understand the ecological and evolutionary drivers of this important genomic trait.

evolutionary biology↗

Shifts in mutation spectra enhance access to beneficial mutations

Biased mutation spectra are pervasive, with wide variation in the magnitude of mutational biases that influence genome evolution and adaptation. How do such diverse biases evolve? Our experiments show that changing the mutation spectrum allows populations to sample previously under-sampled mutational space, including beneficial mutations. The resulting shift in the distribution of fitness effects is advantageous: beneficial mutation supply and beneficial pleiotropy both increase, while deleterious load reduces. More broadly, simulations indicate that reducing or reversing the direction of a long-term bias is always selectively favoured. Such changes in mutation bias can occur easily via altered function of DNA repair genes. A phylogenetic analysis shows that these genes are repeatedly gained and lost in bacterial lineages, leading to frequent bias shifts in opposite directions. Thus, shifts in mutation spectra may evolve under selection, and can directly alter the outcome of adaptive evolution by facilitating access to beneficial mutations. SIGNIFICANCE STATEMENTMutations are important because they provide raw material for evolution. Some types of mutations occur more often than others, and the strength of such mutational bias varies across species. It is not clear how this variation arises. We experimentally measured the immediate effects of changing the mutation bias of E. coli, and used simulations to understand the long-term effects. Altering mutational bias is beneficial whenever the new bias increases sampling of mutational classes that were previously under-sampled. We also show that historically, bacteria have often experienced such beneficial bias switches. Our work thus demonstrates the importance of mutational biases in evolution. By allowing exploration of new mutational space, altered mutation biases could drive rapid adaptation.

evolutionary biology↗

THE IMPACT OF MISTRANSLATION ON PHENOTYPIC VARIABILITY AND FITNESS

Phenotypic variation is widespread in natural populations, and can significantly alter their ecology and evolution. Phenotypic variation often reflects underlying genetic variation, but also manifests via non-heritable mechanisms. For instance, translation errors result in about 10% of cellular proteins carrying altered sequences. Thus, proteome diversification arising from translation errors can potentially generate phenotypic variability, in turn increasing variability in the fate of cells or of populations. However, this link remains unverified. We manipulated mistranslation levels in Escherichia coli, and measured phenotypic variability between single cells (individual level variation), as well as replicate populations (population level variation). Monitoring growth and survival, we find that mistranslation indeed increases variation across E. coli cells, but does not consistently increase variability in growth parameters across replicate populations. Interestingly, although any deviation from the wild type (WT) level of mistranslation reduces fitness in an optimal environment, the increased variation is associated with a survival benefit under stress. Hence, we suggest that mistranslation-induced phenotypic variation can impact growth and survival and has the potential to alter evolutionary trajectories.

evolutionary biology↗

Phenotypic diversity of Methylobacterium associated with rice landraces in Northeast India

The ecology and distribution of many bacteria is strongly associated with specific eukaryotic hosts. However, the impact of such host association on bacterial ecology and evolution is not well understood. Bacteria from the genus Methylobacterium consume plant-derived methanol, and are some of the most abundant and widespread plant-associated bacteria. In addition, many of these species impact plant fitness. To determine the ecology and distribution of Methylobacterium in nature, we sampled bacteria from 36 distinct rice landraces, traditionally grown in geographically isolated locations in North-East (NE) India. These landraces have been selected for diverse phenotypic traits by local communities, and we expected that the divergent selection on hosts may have also generated divergence in associated Methylobacterium strains. We determined the ability of 91 distinct rice-associated Methylobacterium isolates to use a panel of carbon sources, finding substantial variability in carbon use profiles. Consistent with our expectation, across spatial scales this phenotypic variation was largely explained by host landrace identity rather than geographical factors or bacterial taxonomy. However, variation in carbon utilisation was not correlated with sugar exudates on leaf surfaces, suggesting that bacterial carbon use profiles do not directly determine bacterial colonization across landraces. Finally, experiments showed that at least some rice landraces gain an early growth advantage from their specific phyllosphere-colonizing Methylobacterium strains. Together, our results suggest that landrace-specific host-microbial relationships may contribute to spatial structure in rice-associated Methylobacterium in a natural ecosystem. In turn, association with specific bacteria may provide new ways to preserve and understand diversity in one of the most important food crops of the world.

ecology↗

BASAL RESISTANCE AGAINST A PATHOGEN IS MORE BENEFICIAL THAN IMMUNE PRIMING RESPONSES IN FLOUR BEETLES

In insects, basal pathogen resistance and immune priming can evolve as mutually exclusive strategies, with distinct infection outcomes. However, the evolutionary drivers of such diverse immune functions remain poorly understood. Here, we addressed this key issue by systematically analyzing the differential fitness costs and benefits of priming vs. resistance evolution in Tribolium beetle populations infected with Bacillus thuringiensis. Surprisingly, resistant beetles had increased post-infection reproduction and a longer lifespan under both starving as well as fed conditions, with no other measurable costs. In contrast, priming reduced offspring early survival, development rate and reproduction. Priming did improve post-infection survival of offspring, but this added trans-generational benefit of immune priming might not compensate for its pervasive costs. Resistance was thus consistently more beneficial. Our work represents the first report of experimentally evolved trans-generational priming, and a detailed comparison of the complex fitness consequences of evolved priming vs resistance. HIGHLIGHTSO_LIDivergent costs and benefits of experimentally evolved immune priming vs resistance C_LIO_LIIncreased reproduction and lifespan in resistant populations C_LIO_LINo other hidden costs of resistance C_LIO_LIIn contrast, reduced juvenile fitness and reproduction in primed populations C_LIO_LIFirst evidence for experimentally evolved trans-generational immune priming C_LI

evolutionary biology↗

Global mistranslation facilitates sampling of beneficial mutations under stress

Mistranslation is typically deleterious, but can sometimes be beneficial. Although a specific mistranslated protein can confer a short-term benefit in a particular environment, the prevalence of high global mistranslation rates remains puzzling given the large overall cost. Here, we show that generalized mistranslation enhances early E. coli survival under various forms of DNA damage, because it leads to early activation of the DNA damage-induced SOS response. Mistranslating cells therefore maintain larger populations, facilitating later sampling of critical beneficial mutations. Thus, under DNA damage, both basal and induced mistranslation (through genetic or environmental means) increase the number of genetically resistant and phenotypically persistent cells. Surprisingly, mistranslation also increases survival at high temperature. This wide-ranging stress resistance relies on Lon protease, which is revealed as a key effector that induces the SOS response in addition to alleviating proteotoxic stress. The new links between error-prone protein synthesis, DNA damage, and generalised stress resistance indicate surprising coordination between intracellular stress responses, and suggest a novel hypothesis to explain high global mistranslation rates.

evolutionary biology↗

Disrupting butterfly microbiomes does not affect host survival and development

Associations with gut microbes play a crucial role in the physiology, immune function, development, and behavior of many insects. However, butterflies may be an exception to this pattern since butterfly microbiomes do not show the host-specific and developmental shifts that are expected to evolve under strong host-microbial associations. Here, we present the first experimental test of this hypothesis by disrupting gut microbial communities of two butterfly species, Danaus chrysippus and Ariadne merione. Larvae of both the species fed on host plant leaves that were either chemically sterilized or treated with antibiotics had significantly reduced bacterial loads and disrupted gut bacterial communities substantially. However, neither host species treated this way suffered a significant fitness cost. We did not find significant variation in survival, growth and development between test larvae and control larvae. This suggested that butterflies do not rely on their gut bacteria for digestion, detoxification, resource accumulation and metamorphosis. Thus, our results provide empirical support for the growing realization that dependence on gut bacteria for growth and survival is not a universal phenomenon across insects.

ecology↗

Host dietary specialization and neutral assembly shape gut bacterial communities of wild dragonflies

Host-associated gut microbial communities can have large impacts on host ecology and evolution, and are typically shaped by host taxonomy and diet. Different host species often harbor distinct microbial communities, potentially because (1) host dietary specialization determines microbial colonization, (2) host-specific selection acts on diet-acquired microbiota, and (3) a combination of both processes. While the first possibility involves passive community structuring, the other two may arise from a functional association and should produce stable microbial communities. However, these alternatives have rarely been tested in wild host populations. We used 16S rRNA amplicon sequencing to characterize the gut bacterial communities of six dragonfly species collected across multiple seasons and locations. We found that variation in bacterial community composition was predominantly explained by sampling season and location, and secondarily by host species. To distinguish the role of host dietary specialization and host-imposed selection, we used insect-specific primers to identify prey in the gut contents of three focal dragonfly species. We found that these dragonflies - considered to be generalist predators - consumed distinct prey, with seasonal diet variation. Together, the patterns of host dietary specialization and spatial and temporal variation suggest a strong role of passive processes in shaping the gut bacterial community. Indeed, the abundance and distribution of ~76% of the bacterial community members were consistent with neutral community assembly. Our results contradict the pervasive expectation that host-imposed selection shapes gut microbial communities, and highlight the importance of joint analyses of variation in host diet and gut microbial communities of natural host populations.

evolutionary biology↗

Restoring ancestral microbiome aids beetle adaptation to new diets

Eukaryotic hosts often depend on microbes that enhance their fitness, and such relationships may be relatively easily maintained in a stable environment. What is the fate of these associations under rapid environmental change? For instance, if the host switches to a new diet and/or encounters a different microbial community, how does the host-microbiome relationship change? Are the changes adaptive, and how rapidly do they occur? We addressed these questions with the red flour beetle Tribolium castaneum, a generalist insect pest that both consumes and lives in stored grain flour. We found that beetle fitness is enhanced by flour-acquired microbes in the ancestral habitat (wheat flour), but not in novel suboptimal environments (e.g. corn flour) that have a different resident microbial community. Beetles that disperse to new habitats thus have low fitness and a dramatically altered microbiome. Enriching novel habitats with ancestral (wheat-derived) microbes increased beetle fitness, suggesting a viable adaptive strategy. Indeed, within a few generations of laboratory adaptation to two distinct novel habitats, we found that beetle populations gradually restored their ancestral microbiome. Importantly, evolved populations showed a microbe-dependent increase in fecundity and survival on the new diet. We suggest that such repeated, rapid restoration of host-microbe associations may allow generalists to successfully colonize new habitats and escape extinction despite sudden environmental changes.

evolutionary biology↗

Antagonistic pleiotropy is unexpectedly rare in new mutations

Pleiotropic effects of mutations may underlie diverse biological phenomena such as ageing and specialization. In particular, antagonistic pleiotropy (\"AP\": when a mutation has opposite fitness effects in different environments) generates tradeoffs, which may constrain adaptation. Models of adaptation typically assume that AP is common - especially among large-effect mutations - and that pleiotropic effect sizes are positively correlated. The rare empirical tests of these assumptions have largely focused on beneficial mutations observed under strong selection, whereas most mutations are actually deleterious or neutral, and are removed by selection. We quantified the incidence, nature and effect size of pleiotropy for carbon utilization across 80 single mutations in Escherichia coli that arose under mutation accumulation (i.e. weak selection). Although ~46% of the mutations were pleiotropic, only 11% showed AP, which is lower than expected given the distributions of fitness effects for each resource. In some environments, AP was more common in large-effect mutations (but not synergistic pleiotropy, SP); whereas pleiotropic effect sizes were positively correlated for SP (but not AP). Thus, AP is generally rare, is not consistently enriched in large-effect mutations, and often involves weakly deleterious antagonistic effects. Our unbiased quantification of mutational effects therefore suggests that antagonistic pleiotropy is unlikely to cause maladaptive tradeoffs.

evolutionary biology↗

The induction of larval resource preference in heterogeneous habitats

Animals often have to evaluate and choose between multiple food sources in their habitat, and these potentially complex decisions can have a large impact on their fitness. Among other factors, previous experience with an alternative resource can significantly increase subsequent preference for the resource (\"induction of preference\"). Such induction of resource preference is particularly relevant in spatially or temporally heterogeneous habitats. Although most mobile species - especially generalists - probably frequently encounter habitat heterogeneity, the impact of preference induction on individual behaviour and fitness in heterogeneous habitats is poorly understood. We analysed larval preference induction in wheat-adapted generalist red flour beetles (Tribolium castaneum) under three types of habitat heterogeneity. We first analysed the induction of larval preference for novel resources (other cereal flours) under temporal heterogeneity, exposing larvae to new resources during development. We found that larvae preferred a new resource if they experienced it recently, but that the magnitude of induction varied across resources. Interestingly, we also observed specific induction for a homogenous mix of wheat and a novel resource, with larvae preferring the mix over either pure resource. To analyse induction under spatial heterogeneity, we placed beetle eggs in one of two alternative resource patches and tested the preference of emerged larvae. Unexpectedly, hatching into a novel resource did not always induce preference. Finally, we found that induction of preference for new resources could be maladaptive for larval development. Together, our work demonstrates that experience-based plasticity of larval resource choice may strongly impact larval preference and fitness in heterogeneous habitats.

ecology↗

Pathogen susceptibility and fitness costs explain variation in immune priming across natural populations of flour beetles

In many insects, individuals primed with low doses of pathogens live longer after being exposed to the same pathogen later in life. Yet, our understanding of the evolutionary and ecological history of priming of immune response in natural insect populations is limited. Previous work demonstrated population-, sex- and- stage specific variation in the survival benefit of priming response in flour beetles (Tribolium castaneum) infected with their natural pathogen Bacillus thuringiensis. However, the evolutionary forces responsible for this natural variation remained unclear. Here, we tested whether the strength of the priming response (measured as the survival benefit after priming and subsequent infection relative to unprimed controls) was associated with multiple fitness parameters across 10 flour beetle populations. Our results suggest two major selective pressures that may explain the observed inter-population variation in priming: (A) Basal pathogen susceptibility - populations that were more susceptible to infection produced a stronger priming response, and (B) Reproductive success - populations where primed females produced more offspring had lower survival benefit, suggesting a trade-off between priming response and reproduction. Our work is the first empirical demonstration of multiple selective pressures that may govern the adaptive evolution of immune priming in the wild. We hope that this motivates further experiments to establish the role of pathogen-imposed selection and fitness costs in the evolution of priming in natural insect populations.

evolutionary biology↗

The Evolutionary History and Impact of Bacterial tRNA Modifications

Along with tRNAs, enzymes that modify anticodon bases are a key aspect of translation across the tree of life. tRNA modifications extend wobble pairing, allowing specific (\"target\") tRNAs to recognize multiple codons and cover for other (\"non-target\") tRNAs, often improving translation efficiency and accuracy. However, the detailed evolutionary history and impact of tRNA modifying enzymes has not been analyzed. Using ancestral reconstruction of five tRNA modifications across 1093 bacteria, we show that most modifications were ancestral to eubacteria, but were repeatedly lost in many lineages. Most modification losses coincided with evolutionary shifts in non-target tRNAs, often driven by increased bias in genomic GC and associated codon use, or by genome reduction. In turn, the loss of tRNA modifications stabilized otherwise highly dynamic tRNA gene repertoires. Our work thus traces the complex history of bacterial tRNA modifications, providing the first clear evidence for their role in the evolution of bacterial translation.

evolutionary biology↗

DIETARY AND DEVELOPMENTAL SHIFTS IN BUTTERFLY-ASSOCIATED BACTERIAL COMMUNITIES

Bacterial communities associated with insects can substantially influence host ecology, evolution and behavior. Host diet is a key factor that shapes bacterial communities, but the impact of dietary transitions across insect development is poorly understood. We analyzed bacterial communities of 12 butterfly species across different development stages, using 16S rDNA amplicon sequencing. Butterfly larvae typically consume leaves of a single host plant, whereas adults are more generalist nectar feeders. Thus, we expected bacterial communities to vary substantially across butterfly development. Surprisingly, very few species showed significant developmental transitions in bacterial communities, suggesting weak impacts of dietary transitions across butterfly development. On the other hand, bacterial communities were strongly influenced by butterfly species identity and dietary variation across species. Larvae of most butterfly species largely mirrored bacterial community composition of their diets, suggesting passive acquisition rather than active selection. Overall, our results suggest that although butterflies harbor distinct microbiomes across taxonomic groups and dietary guilds, the dramatic dietary shifts that occur during development do not impose strong selection to maintain distinct bacterial communities.

ecology↗

Experimental Evolution Of Insect Immune Memory Vs. Pathogen Resistance

Under strong pathogen pressure, insects often evolve resistance to infection. Many insects are also protected via immune memory ( immune priming), whereby sub-lethal exposure to a pathogen enhances survival after secondary infection. To understand the evolution and consequences of these immune responses, we imposed strong pathogen selection on flour beetles (Tribolium castaneum), infecting them with Bacillus thuringiensis (Bt) for 11 generations. Populations injected first with heat-killed and then live Bt each generation evolved high basal resistance against multiple Bt strains. In contrast, all populations injected only with a high dose of live Bt evolved less effective but strain-specific priming response. Control populations injected with heat-killed Bt did not evolve priming; and in the ancestor, priming was effective only against a low Bt dose. Thus, pathogens can select for rapid modulation of insect priming ability, leading to divergent immune strategies (generalized resistance vs. specific immune priming) with distinct mechanisms and adaptive benefits.

evolutionary biology↗

FEMALE CHEMICAL WARFARE DRIVES FITNESS EFFECTS OF GROUP SEX RATIO

In animals, skewed sex ratios can affect individual fitness either via sexual interactions (e.g. intersexual conflict or intrasexual mate competition) or non-sexual interactions (e.g. sex-specific resource competition). Because most analyses of sex ratio focus on sexual interactions, the relative importance of these mechanisms remains unclear. We addressed this problem using the flour beetle Tribolium castaneum, where male-biased sex ratios increase female fitness relative to unbiased or female-biased groups. Although flour beetles show both sexual and non-sexual (resource) competition, we found that sexual interactions did not explain female fitness. Instead, female fecundity was dramatically reduced even after a brief exposure to flour conditioned by other females. Earlier studies suggested that quinones (secreted toxins) might mediate density-dependent population growth in flour beetles. We identified ethyl- and methyl-benzoquinone (EBQ and MBQ) as the primary components of adult stink glands that regulate female fecundity. In female-biased groups (i.e. at high female density), females upregulated quinones and suppressed each others reproduction. In male-biased groups, low female density lead to low quinone levels, allowing higher fecundity. Thus, quinones serve both as indicators and mediators of female competition, resulting in the observed fitness decline in female-biased groups. Our results underscore the importance of non-sexual interference competition that may often underlie the fitness consequences of skewed sex ratios.

evolutionary biology↗