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Baur, J.

Publications and source records attributed to Baur, J..

11 recordsLinked to original sources

Environmental predictability favours adaptive behavioural plasticity and relaxes selection against deleterious alleles

Behavioural plasticity can play a key role in evolution by either facilitating or impeding genetic adaptation. The latter occurs when behaviours mitigate selection pressures that otherwise would target associated traits. Therefore, environments that facilitate adaptive behavioural plasticity could relax the strength of natural selection, but experimental evidence for this prediction remains scarce. Here, we first demonstrate that maternal care in the beetle Callosobruchus maculatus is dependent on environmental cues that allow females to reduce larval competition via learning and informed oviposition choices. We show that this facilitation of maternal care relaxes selection against deleterious alleles in offspring. We further find that mothers of low genetic quality generally provide poorer care. However, when receiving environmental cues providing accurate information about future host-quality, the increased opportunity for adaptive behavioural plasticity reduced genetic differences in maternal care, further relaxing selection against deleterious alleles. We use our data to illustrate how the identified link between adaptive behavioural plasticity in maternal care and the strength of natural selection can impact indirect genetic effects between mothers and offspring and the accumulation of cryptic genetic loads in populations inhabiting environments that differ in their predictability.

animal behavior and cognition↗

Strong Selection, but low repeatability: Temperature-specific effects on genomic predictions of adaptation

Climate warming is threatening biodiversity by increasing temperatures beyond the optima of many ectotherms. Due to the inherent non-linear relationship between temperature and the rate of cellular processes, such shifts towards hot temperature are predicted to impose stronger selection compared to corresponding shifts toward cold temperature. This suggests that when adaptation to warming occurs, it should be relatively rapid and predictable. Here, we tested this hypothesis from the level of single-nucleotide polymorphisms to life-history traits, by conducting an evolve-and-resequence experiment on three genetic backgrounds of the beetle, Callosobruchus maculatus. Indeed, phenotypic evolution was faster and more repeatable at hot, relative to cold, temperature. However, at the genomic level, adaptation to heat was less repeatable when compared across genetic backgrounds. As a result, genomic predictions of phenotypic adaptation in populations exposed to hot temperature were accurate within, but not between, backgrounds. These results seem best explained by genetic redundancy and an increased importance of epistasis during adaptation to heat, and imply that the same mechanisms that exert strong selection and increase repeatability of phenotypic evolution at hot temperature, reduce repeatability at the genomic level. Thus, predictions of adaptation in key phenotypes from genomic data may become increasingly difficult as climates warm.

evolutionary biology↗

Life-history adaptation under climate warming magnifies the agricultural footprint of a cosmopolitan insect pest

Climate change is affecting population growth rates of ectothermic pests with potentially dire consequences for agriculture, but how rapid genetic adaptation impacts these dynamics remains unclear. To address this challenge, we predicted how climate change adaptation in life-history traits of insect pests may affect future agricultural yields by unifying thermodynamics based on first principles with classic life-history theory. Our model predicts that warming temperatures favour changes in resource allocation decisions coupled with increased larval host consumption, resulting in a predicted double-blow on agricultural yields under future climate change. We find support for these predictions by studying thermal adaptation in life-history traits and underlying gene expression in the wide-spread insect pest, Callosobruchus maculatus, with five years of life-history evolution under experimental warming causing an almost two-fold increase in its predicted agricultural footprint. These results emphasize the need for integrating a mechanistic understanding of life-history evolution into forecasts of pest impact.

ecology↗

Coevolution of longevity and female care of male gametes

An often-overlooked aspect of life-history optimization is the allocation of resources to protect the germline and secure safe transmission of genetic information. While failure to do so renders significant fitness consequences in future generations, germline maintenance comes with substantial costs. Thus, germline allocation should trade-off with other life history decisions and be optimized in accordance with an organisms reproductive schedule. Here we tested this hypothesis by studying germline maintenance in lines of seed beetle, selected for early (E) or late (L) reproduction for 350 and 240 generations, respectively. Female animals provide maintenance and screening of male gametes in their reproductive tract and oocytes. Here, we revealed the ability of young and aged E and L-females to provide this form of germline maintenance by mating them to males with ejaculates with artificially elevated levels of protein and DNA damage. We find that germline maintenance in E-females peaks at young age and then declines, while the opposite is true for L-females, in accordance with the age of reproduction in respective regime. These findings identify the central role of allocation to secure germline integrity in life history evolution and highlight how females can play a crucial role in mitigating effects of male germline decisions on mutation rate and offspring quality.

evolutionary biology↗

Heat stress reveals a fertility debt owing to postcopulatory sexual selection

Climates are changing rapidly, demanding equally rapid adaptation of natural populations. Whether sexual selection can aid such adaptation is under debate; while sexual selection should promote adaptation when individuals with high mating success are also best adapted to their local surroundings, the expression of sexually selected traits can incur costs. Here we asked what the demographic consequences of such costs may be once climates change to become harsher and the strength of natural selection increases. We investigated how an evolutionary history of strong postcopulatory sexual selection (sperm competition) affects male fertility under acute adult heat stress. Harnessing the empirical potential of long-term experimental evolution in the seed beetle Callosobruchus maculatus, we assessed the thermal sensitivity of fertility (TSF) in replicated lines maintained for 68 generations under three alternative mating regimes manipulating the opportunity for sexual and natural selection. We find that males evolving under strong sexual selection suffer from increased TSF, and that male success in sperm competition (P2: sperm offense) is genetically correlated to increased TSF. Interestingly, females from the regime under strong sexual selection, who experienced relaxed selection on their own reproductive effort, had high fertility in benign settings but suffered increased TSF, like their brothers. This implies that female fertility and TSF evolved through genetic correlation with reproductive traits sexually selected in males. Paternal but not maternal heat stress reduced offspring fertility with no evidence for adaptive transgenerational plasticity among heat-exposed offspring, indicating that the observed effects may compound over generations. Our results suggest that trade-offs between fertility and traits increasing success in postcopulatory sexual selection can be revealed in harsh environments. This can put polyandrous species under increased risk during extreme heat waves expected under future climate change. IMPACT STATEMENTHow will populations respond to a warming world? Of increasing concern are negative effects of elevated temperatures on fertility, which in many species are observed for temperatures substantially lower than the ones causing death. Incorporating knowledge on species-specific thermal fertility limits has improved estimates of current species ranges but renders a more pessimistic view of the potential for adaptive responses under climate change. Sexual selection is a process that can interact with thermal sensitivity of fertility and is strongest in males of polyandrous species, in which females mate multiply and sperm of multiple males compete for fertilization of female eggs. Therefore, males of polyandrous species often invest heavily in sperm competition. However, given finite resources, increased investment in sperm competition can come at an expense of other processes needed to maintain the integrity of the male germline, which when compromised can reduce fertility and offspring quality. How may such male investment, fuelled by sexual selection, affect species responses to climate warming? To address this question, we first evolved populations under different laboratory settings that independently manipulated the levels of natural and sexual selection. We exposed adults from these populations to acute heat stress and measured the fertility of males and females. We find that sexual selection on males leads to a fertility debt that is revealed under heat stress. This debt was also apparent in females, who themselves were not selected for increased reproductive investment. Thus, genes under sexual selection in males seems to have impaired fertility in both sexes under heat stress. Forecasts of species response to climate change that do not incorporate thermal fertility limits and sexual selection may therefore underestimate species vulnerability to increasing temperatures.

evolutionary biology↗

Telomere dysfunction impairs intestinal differentiation andpredisposes to diet-induced colitis

Intestinal epithelium dysfunction causes barrier defects, malabsorption and dysbiosis, predicting local and systemic disease, morbidity and mortality in humans. However, the underlying causes are not well understood. Here we show that telomere shortening is a host intrinsic factor that impairs enterocyte differentiation. The presence of such undifferentiated enterocytes is associated with barrier disruption and malabsorption of nutrients, such as fructose. A fructose-rich diet causes increased fructose spillover to the colon and induces colitis in a microbiome-dependent manner. The microbiome uses fructose to synthesize essential metabolites, including NAD precursors, that complement the hosts low NAD pool in the inflamed colon. Thus, telomere shortening drives enterocyte dysfunction and predisposes to diet-induced colitis through barrier disruption, increased nutrient flux to the colon and modulation of the microbiome. This differerentiation defect expands the canonical stem cell failure-centered view of how telomere shortening impacts the intestine and predisposes to intestinal disease in conditions associated with short telomeres.

cell biology↗

Increased male investment in sperm competition results in offspring of lower quality

Male animals often show higher mutation rates than their female conspecifics. A hypothesis for this male-bias is that competition over fertilization of female gametes leads to increased male investment into reproduction at the expense of maintenance and repair, resulting in a trade-off between male success in sperm competition and offspring quality. Here, we provide evidence for this hypothesis by harnessing the power of experimental evolution to study effects of sexual selection on the male germline in the seed beetle Callosobruchus maculatus. We first show that 50 generations of evolution under strong sexual selection, coupled with experimental removal of natural selection resulted in males that are more successful in sperm competition. We then show that these males produce progeny of lower quality if engaging in socio-sexual interactions prior to being challenged to surveil and repair experimentally induced damage in their germline, and that the presence of male competitors alone can be enough to elicit this response. We identify 18 candidate genes that showed differential expression in response to the induced germline damage, with several of these previously implicated in processes associated with DNA repair and cellular maintenance. These genes also showed significant expression changes across socio-sexual treatments of fathers and predicted the reduction in quality of their offspring, with expression of one gene also being strongly correlated to male sperm competition success. Sex differences in expression of the same 18 genes indicate a substantially higher female investment in germline maintenance. While more work is needed to detail the exact molecular underpinnings of our results, our findings provide rare experimental evidence for a trade-off between male success in sperm competition and germline maintenance. This suggests that sex-differences in the relative strengths of sexual and natural selection are causally linked to male mutation bias. The tenet advocated here, that the choices of an individual can affect plasticity of its germline and the resulting genetic quality of subsequent generations, has several interesting implications for mate choice processes.

evolutionary biology↗

The mating system affects the temperature sensitivity of male and female fertility

O_LITo mitigate effects of climate change it is important to understand species responses to increasing temperatures. This has often been done by studying survival or activity at temperature extremes. Before such extremes are reached, however, effects on fertility may already be apparent. C_LIO_LISex differences in the thermal sensitivity of fertility (TSF) could impact species persistence under climate warming because female fertility is typically more limiting to population growth than male fertility. However, little is known about sex differences in TSF. C_LIO_LIHere we first demonstrate that the mating system can strongly influence TSF using the seed beetle Callosobruchus maculatus. We exposed populations carrying artificially induced mutations to two generations of short-term experimental evolution under alternative mating systems, manipulating the opportunity for natural and sexual selection on the mutations. We then measured TSF in males and females subjected to juvenile or adult heat stress. C_LIO_LIPopulations kept under natural and sexual selection had higher fitness, but similar TSF, compared to control populations kept under relaxed selection. However, females had higher TSF than males, and strikingly, this sex difference had increased over only two generations in populations evolving under sexual selection. C_LIO_LIWe hypothesized that an increase in male-induced harm to females during mating had played a central role in driving this evolved sex difference, and indeed, remating under conditions limiting male harassment of females reduced both male and female TSF. Moreover, we show that manipulation of mating system parameters in C. maculatus generates intraspecific variation in the sex difference in TSF equal to that found among a diverse set of studies on insects. C_LIO_LIOur study provides a causal link between the mating system and TSF. Sexual conflict, (re)mating rates, and genetic responses to sexual selection differ among ecological settings, mating systems and species. Our study therefore also provides mechanistic understanding for the variability in previously reported TSFs which can inform future experimental assays and predictions of species responses to climate warming. C_LI

ecology↗

Sexual conflict drives micro- and macroevolution of sexual dimorphism in immunity

BackgroundSexual selection can have major effects on mating rates and sex-specific costs of mating and may thereby influence sex-differences in immunity as well as associated host-pathogen dynamics. Yet, experimental evidence linking the mating system to evolved sexual dimorphism in immunity are scarce and the direct effects of mating rate on immunity are not well established. Here, we use transcriptomic analyses, experimental evolution and phylogenetic comparative methods to study the association between the mating system and sexual dimorphism in immunity in seed beetles, where mating causes internal injuries in females. ResultsWe demonstrate that female phenoloxidase (PO) activity, involved in wound healing and defence against parasitic infections, is elevated relative to males. This difference is accompanied by concomitant sex-differences in the expression of genes in the pro-phenoloxidase activating cascade. We document substantial phenotypic plasticity in female PO activity in response to mating and show that experimental evolution under enforced monogamy (resulting in low remating rates and sexual conflict relative to natural polygamy) rapidly decreases female (but not male) PO activity. Moreover, monogamous females have evolved increased tolerance to bacterial infection unrelated to mating, implying that female responses to costly mating may trade off with other aspects of immune defence, an hypothesis which broadly accords with the documented sex differences in gene expression. Finally, female (but not male) PO activity shows correlated evolution with the perceived harmfulness of male genitalia across 12 species of seed beetles, suggesting that sexual conflict has a significant influence on sexual dimorphisms in immunity in this group of insects. ConclusionsOur study provides insights into the links between sexual conflict and sexual dimorphism in immunity at the molecular and phenotypic level and suggests that selection pressures moulded by mating interactions can lead to a sex-specific mosaic of immune responses with important implications for host-pathogen dynamics in sexually reproducing organisms.

evolutionary biology↗

Quantitative fluxomics of circulating metabolites

Mammalian organs are nourished by nutrients carried by the blood circulation. These nutrients originate from diet and internal stores, and can undergo various interconversions before their eventual use as tissue fuel. Here we develop isotope tracing, mass spectrometry, and mathematical analysis methods to determine the direct sources of circulating nutrients, their interconversion rates, and eventual tissue-specific contributions to TCA cycle metabolism. Experiments with fifteen nutrient tracers enabled extensive accounting both for circulatory metabolic cycles and tissue TCA inputs, across fed and fasted mice on either high carbohydrate or ketogenic diet. We find that a majority of circulating carbon flux is carried by two major cycles: glucose-lactate and triglyceride-glycerol-fatty acid. Futile cycling through these pathways is prominent when dietary content of the associated nutrients is low, rendering internal metabolic activity robust to food choice. The presented in vivo flux quantification methods are broadly applicable to different physiological and disease states.

systems biology↗

Sexual selection and the evolution of male and female cognition: a test using experimental evolution in seed beetles

\"The mating mind hypothesis\", originally aimed at explaining human cognition, holds that the socio-sexual environment shapes cognitive abilities among animals. Similarly, general sexual selection theory predicts that mate competition should benefit individuals carrying \"good genes\" with beneficial pleiotropic effects on general cognitive ability. However, few experimental studies have evaluated these related hypotheses due to difficulties of performing direct tests in most taxa. Here we harnessed the empirical potential of the seed beetle study system to investigate the role of sexual selection and mating system in the evolution of cognition. We evolved replicate lines of beetle under enforced monogamy (eliminating sexual selection) or polygamy for 35 generations and then challenged them to locate and discriminate among mating partners (male assays) or host seeds (female assays). To assess learning, the same beetles performed the task in three consecutive rounds. All lines learned the task, improving both within and between trails. Moreover, polygamous males outperformed monogamous males. However, there were no differences in the rate of learning between males of the two regimes, and polygamous females showed no improvement in host search, and even signs of reduced learning. Hence, while sexual selection was a potent factor that increased cognitive performance in mate search, it did not lead to the general increase in cognitive abilities expected under the \"mating mind\" hypothesis or general \"good genes\" theory. Our results highlight sexually antagonistic (balancing) selection as a potential force maintaining genetic variation in cognitive traits.

animal behavior and cognition↗