@article {160485, title = {Founders predict trait evolution and population performance after evolutionary rescue in the red flour beetle.}, journal = {Proc Natl Acad Sci U S A}, volume = {122}, year = {2025}, month = {2025 Sep 09}, pages = {e2506244122}, abstract = {

Evolutionary rescue helps populations survive environmental change, but the phenotypic and demographic factors associated with rescue dynamics and its long-term effects remain unclear. We experimentally evolved 10 wild-collected populations of flour beetles from across India in a suboptimal corn resource for 70 generations (\>5 y), collecting \>10,000 population census points book-ended by measurements of fitness-related traits for 30 experimental lines. Despite clear ancestral trait differences, all lines showed highly parallel evolutionary rescue within 20 generations. Long-term average population size varied across source populations and was positively correlated with ancestral development rate, which increased convergently across populations and emerged as the single best predictor of population performance during and after evolutionary rescue. Notably, specific demographic events during rescue (such as the rate of population decline and recovery) were uncorrelated both with ancestral trait distributions and post-rescue adaptation. Our results support prior work showing founder traits as key predictors of adaptation, and highlight their role in long-term adaptation and trait evolution following evolutionary rescue.

}, keywords = {Adaptation, Physiological, Animals, Biological Evolution, Coleoptera, India, Phenotype, Population Density, Population Dynamics}, issn = {1091-6490}, doi = {10.1073/pnas.2506244122}, author = {Ravi Kumar, Vrinda and Buddh, Shyamsunder and Singhal, Shivansh and Prakash, Arun and Agashe, Deepa} } @article {134602, title = {Alteration of diet microbiota limits the experimentally evolved immune priming response in flour beetles, but not pathogen resistance.}, journal = {J Evol Biol}, year = {2023}, month = {2023 Sep 01}, abstract = {

Host-associated microbiota play a fundamental role in the training and induction of different forms of immunity, including inducible as well as constitutive components. However, direct experiments analysing the relative importance of microbiota on diverse forms of evolved immune functions are missing. We addressed this gap by using experimentally evolved lines of Tribolium castaneum that either produced inducible immune memory-like responses (immune priming) or constitutively expressed basal resistance (without priming), as divergent counterstrategies against Bacillus thuringiensis infection. We altered the microbial communities present in the diet (i.e. wheat flour) of these evolved lines using UV irradiation and estimated the impact on the beetle{\textquoteright}s ability to mount a priming response versus basal resistance. Populations that had evolved immune priming lost the ability to mount a priming response upon alteration of diet microbiota. Microbiota manipulation also caused a drastic reduction in their reproductive output and post-infection longevity. In contrast, in pathogen-resistant beetles, microbiota manipulation did not affect post-infection survival or reproduction. The divergent evolution of immune responses across beetle lines was thus associated with divergent reliance on the microbiome. Whether the latter is a direct outcome of differential pathogen exposure during selection or reflects evolved immune functions remains unclear. We hope that our results will motivate further experiments to understand the mechanistic basis of these complex evolutionary associations between microbiota, host immune strategies and fitness outcomes.

}, issn = {1420-9101}, doi = {10.1111/jeb.14213}, author = {Prakash, Arun and Agashe, Deepa and Khan, Imroze} } @article {99928, title = {The costs and benefits of basal infection resistance vs immune priming responses in an insect.}, journal = {Dev Comp Immunol}, volume = {126}, year = {2022}, month = {2021 Sep 16}, pages = {104261}, abstract = {

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. Overall, our work demonstrates the evolutionary change in trans-generational priming response, and provides a detailed comparison of the complex fitness consequences of evolved priming vs resistance.

}, issn = {1879-0089}, doi = {10.1016/j.dci.2021.104261}, author = {Prakash, Arun and Agashe, Deepa and Khan, Imroze} } @article {59711, title = {Pathogen susceptibility and fitness costs explain variation in immune priming across natural populations of flour beetles.}, journal = {J Anim Ecol}, year = {2019}, month = {2019 May 27}, abstract = {

In many insects, individuals primed with low doses of pathogens early in life have higher survival after exposure 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. In the present work, 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 and immune components across 10 flour beetle populations collected from different locations in India. 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) Short-term early reproductive success - populations where primed females produced more offspring early in life (measured over 2\ days) had lower survival benefit (measured over 120\ days), suggesting a potential trade-off between early reproduction and priming response. However, the negative association between survival and reproduction is limited to priming and infection in adults, but not in larvae. While other components of beetle fitness (starvation resistance and larval development) and immune function (haemolymph antibacterial activity and antimicrobial quinone secretion) also varied widely across populations, none of them was correlated with the variation in priming responses across populations. Our work is the first systematic empirical demonstration of multiple selective pressures that may govern the 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.

}, issn = {1365-2656}, doi = {10.1111/1365-2656.13030}, author = {Khan, Imroze and Prakash, Arun and Agashe, Deepa} } @article {27663, title = {Female Density-Dependent Chemical Warfare Underlies Fitness Effects of Group Sex Ratio in Flour Beetles}, journal = {American Naturalist}, year = {2018}, month = {12/2017}, abstract = {

In animals, skewed sex ratios can affect individual fitness via sexual (e.g., intersexual conflict or intrasexual mate competition) or nonsexual (e.g., sex-specific resource competition) interactions. Because most analyses of sex ratio focus on sexual interactions, the relative importance of sexual versus nonsexual mechanisms remains unclear. We tested both mechanisms in 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 nonsexual (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 secreted toxins might mediate density-dependent population growth in flour beetles. We identified ethyl benzoquinone and methyl benzoquinone (quinones) as 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 other{\textquoteright}s reproduction. In male-biased groups, low female density and associated low quinone levels maximized fecundity. Thus, females appear to use quinones as weapons for female-specific, density-dependent interference competition. Our results underscore the importance of nonsexual interference competition that may often underlie the fitness consequences of skewed sex ratios.

}, doi = {10.1086/695806}, author = {Khan, Imroze and Prakash, Arun and Issar, Swastika and Umarani, Mihir and Sasidharan, Rohit and Masagalli, JN and Lama, Prakash and Venkatesan, Radhika and Agashe, Deepa} } @article {27662, title = {Experimental evolution of insect immune memory versus pathogen resistance.}, journal = {Proc Biol Sci}, volume = {284}, year = {2017}, month = {2017 Dec 20}, abstract = {

Under strong pathogen pressure, insects often evolve resistance to infection. Many insects are also protected via immune memory (immune priming), whereby sublethal exposure to a pathogen enhances survival after secondary infection. Theory predicts that immune memory should evolve when the pathogen is highly virulent, or when pathogen exposure is relatively rare. However, there are no empirical tests of these hypotheses, and the adaptive benefits of immune memory relative to direct resistance against a pathogen are poorly understood. To determine the selective pressures and ecological conditions that shape immune evolution, we imposed strong pathogen selection on flour beetle (Tribolium castaneum) populations, infecting them with Bacillus thuringiensis (Bt) for 11 generations. Populations injected first with heat-killed and then live Bt evolved high basal resistance against multiple Bt strains. By contrast, populations injected only with a high dose of live Bt evolved a 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. Intriguingly, one replicate population first evolved priming and subsequently evolved basal resistance, suggesting the potential for dynamic evolution of different immune strategies. Our work is the first report showing that pathogens can select for rapid modulation of insect priming ability, allowing hosts to evolve divergent immune strategies (generalized resistance versus specific immune memory) with potentially distinct mechanisms.

}, issn = {1471-2954}, doi = {10.1098/rspb.2017.1583}, author = {Khan, Imroze and Prakash, Arun and Agashe, Deepa} } @article {11618, title = { Divergent immune priming responses across flour beetle life stages and populations }, journal = { ECOLOGY AND EVOLUTION }, volume = {6}, year = {2016}, month = {11/2016}, pages = {7847-7855}, abstract = {

Growing evidence shows that low doses of pathogens may prime the immune response in many insects, conferring subsequent protection against infection in the same developmental stage (within-life stage priming), across life stages (ontogenic priming), or to offspring (transgenerational priming). Recent work also suggests that immune priming is a costly response. Thus, depending on host and pathogen ecology and evolutionary history, tradeoffs with other fitness components may constrain the evolution of priming. However, the relative impacts of priming at different life stages and across natural populations remain unknown. We quantified immune priming responses of 10 natural populations of the red flour beetle Tribolium castaneum, primed and infected with the natural insect pathogen Bacillus thuringiensis. We found that priming responses were highly variable both across life stages and populations, ranging from no detectable response to a 13-fold survival benefit. Comparing across stages, we found that ontogenic immune priming at the larval stage conferred maximum protection against infection. Finally, we found that various forms of priming showed sex-specific associations that may represent tradeoffs or shared mechanisms. These results indicate the importance of sex-, life stage-, and population-specific selective pressures that can cause substantial divergence in priming responses even within a species. Our work highlights the necessity of further work to understand the mechanistic basis of this variability.

}, doi = {10.1002/ece3.2532}, author = {Khan, Imroze and Prakash, Arun and Agashe, Deepa} } @article {1028, title = {Immunosenescence and the ability to survive bacterial infection in the red flour beetle Tribolium castaneum.}, journal = {J Anim Ecol}, volume = {85}, year = {2016}, month = {01/2016}, pages = {291-301}, abstract = {

In most animals, ageing is associated with a decline in immune function (immune senescence). However, different components of the immune system seem to age differentially, and many studies do not measure the ultimate fitness consequences of immune function after infection. Previous work shows that immune function may be traded off with other fitness components such as reproduction. It is possible that age alters the nature of these trade-offs, particularly in conjunction with factors such as gender and mating that can also affect investment in immune function. We tested the impact of age, sex and mating on post-infection survivorship in Tribolium castaneum flour beetles, as well as the components of baseline constitutive innate immunity and external (secreted) immune function in uninfected individuals. We also tested whether the reproductive ability of uninfected females is traded off with immune function (baseline innate and external immunity) and post-infection survivorship across age groups. We found that age, sex and mating significantly affected immune components and infection outcome, although the magnitude and nature of the impact varied in each case. We found that older beetles were more susceptible to infection by the pathogen Bacillus thuringiensis even though major components of the constitutive innate immune defence (antibacterial and phenoloxidase activity) remained unchanged or improved with age. Thus, these aspects of innate immunity cannot explain the observed decline in post-infection survival of older beetles. We did not find trade-offs between the reproductive ability of uninfected females and their immune function. In contrast to innate immunity, external immunity showed an overall decline with age but was also affected by sex and mating. Finally, we show that bacterial infection alters external immunity via complex interactions between age, sex and mating status. Our work uncovers novel interactions between age, sex and mating that can determine the evolution and outcome of immunosenescence by affecting the time course of relative investment in different immune and fitness components.

}, issn = {1365-2656}, doi = {10.1111/1365-2656.12433}, author = {Khan, Imroze and Prakash, Arun and Agashe, Deepa} }