Search bioRxiv⌕ Search

Biology subjects

Chapman, T.

Publications and source records attributed to Chapman, T..

28 records · Page 2Linked to original sources

Reproductive plasticity in both sexes interacts to determine mating behaviour and fecundity

Organisms alter their phenotype in response to variation in their environment by expressing phenotypic plasticity. Both sexes exhibit such plasticity in response to contrasting environmental and social cues, and this can reflect the influence of sexual conflict. However, theory predicts that plasticity expressed by both sexes may either maximise the sex-specific fitness of both, or of one sex at the expense of the other. Hence empirical tests of the predictions are sorely needed. Here we conducted novel tests of the fitness effects of interacting reproductive plasticity in Drosophila melanogaster. First, prior to mating, males were kept alone, or with same sex rivals, and females were kept alone, in same sex, or mixed sex groups. Second, we conducted matings between individuals from all these social treatments under choice and no choice scenarios. The results showed that males and females can both plastically respond to these socio-sexual environments to influence the expression of mating duration, mating latency, and fecundity. These plastic responses interacted significantly to determine mating latency and fecundity. Effects on mating latency were also observed under both choice and no-choice conditions, but in opposing directions. Variation in the outcome of interacting plasticity pivoted around the outcomes observed with focal females that had been maintained in same-sex environments prior to mating. However, not all fitness-related traits examined responded in the same way. Mating duration was determined largely by the social environment of the male. Our results show that the expression of some, but not all fitness-related reproductive traits can be determined by the outcome of interacting behavioural plasticity expressed by both sexes. This highlights the need for new predictive theory informed by these empirically-derived parameters. Overall, we conclude that variation in the expression of shared traits due to interacting plasticity represents an important and novel facet of sexual interactions. Impact SummaryAnimals and plants are able to respond to variation in their environment by expressing phenotypic plasticity. In sexual organisms, both males and females can exhibit such plasticity but the cues they respond to and the fitness consequences of these actions may be different between the sexes, and even conflicting. For example, males may respond to the presence of competitors by altering their mating behaviour or ejaculate transfer to increase their own, but not necessarily their mates reproductive output. However, females may also express phenotypic plasticity in response to their social and sexual environment to maximise their own fitness. Theory suggests that plasticity expressed by both sexes may either maximise the sex-specific fitness of both, or of one sex at the expense of the other. So far, little experimental work has been conducted to explore such interacting plasticity. Here we conducted novel tests of the fitness effects of interacting plasticity in the fruit fly Drosophila melanogaster. In doing so, we provide novel experimental evidence for interacting behavioural plasticity. We show that males and females can plastically respond to their socio-sexual environment to influence the expression of mating duration, mating latency, and fecundity. These plastic responses, while induced to increase the fitness interests of each sex, interact in the case of mating latency and fecundity and may reflect the outcome of sexual conflict. Our findings suggest that studies of reproductive behaviour should carefully consider the socio-sexual environment of both males and females and highlight the need for new predictive theory informed by empirically-derived parameters. Overall, we show that interacting plasticity between sexes represents an important and novel facet of sexual interactions.

evolutionary biology↗

Rats strategically manage learning during perceptual decision making

Balancing the speed and accuracy of decisions is crucial for survival, but how organisms manage this trade-off during learning is largely unknown. Here, we track this trade-off during perceptual learning in rats and simulated agents. At the start of learning, rats chose long reaction times that did not optimize instantaneous reward rate, but by the end of learning chose near-optimal reaction times. To understand this behavior, we analyzed learning dynamics in a recurrent neural network model of the task. The model reveals a fundamental trade-off between instantaneous reward rate and perceptual learning speed, putting the goals of learning quickly and accruing immediate reward in tension. We find that the rats strategy of long initial responses can dramatically expedite learning, yielding higher total reward over task engagement. Our results demonstrate that prioritizing learning can be advantageous from a total reward perspective, and suggest that rats engage in cognitive control of learning.

neuroscience↗

Reduced insulin signalling in adulthood protects soma and germline under mutation accumulation

Adulthood-only downregulation of insulin/IGF-1 signalling (IIS), an evolutionarily conserved pathway regulating resource allocation between somatic maintenance and reproduction, increases lifespan without fecundity cost in the nematode, Caenorhabditis elegans. However, long-term multigenerational effects of reduced IIS remain unexplored and are proposed to carry costs for offspring quality. To test this hypothesis, we ran a mutation accumulation (MA) experiment and downregulated IIS in half of the 400 MA lines by silencing daf-2 gene expression using RNA interference (RNAi) across 40 generations. Contrary to the prediction, adulthood-only daf-2 RNAi reduced extinction of MA lines both under UV-induced and spontaneous mutation accumulation. Fitness of the surviving UV-induced MA lines was higher under daf-2 RNAi. Reduced IIS increased intergenerational F1 offspring fitness under UV stress but had no quantifiable transgenerational effects. Functional hrde-1 was required for the benefits of multigenerational daf-2 RNAi. Overall, we found net benefit to fitness from multigenerational reduction of IIS and the benefits became more apparent under stress. Because reduced daf-2 expression during development carries fitness costs, we suggest that our findings are best explained by the developmental theory of ageing, which maintains that the decline in the force of selection with age results in poorly regulated gene expression in adulthood.

evolutionary biology↗

Transmission efficiency drives host-microbe associations

Sequencing technologies have fueled a rapid rise in descriptions of microbial communities associated with hosts, but what is often harder to ascertain is their evolutionary significance. Here we review the existing literature on the role of vertical (VT), horizontal (HT), environmental acquisition, and mixed modes (MMT) of transmission for establishing animal host-microbe associations. We then modelled four properties of gut microbiota proposed as key to promoting animal host-microbe relationships: modes of transmission, host reproductive mode, host mate choice, and host fitness. We found: (i) MMT led to the highest frequencies of host-microbe associations, and some environmental acquisition or HT of microbes was required for persistent associations to form unless VT was perfect; (ii) host reproductive mode (sexual vs asexual) and host mate choice (for microbe carriers vs non-carriers) had little impact on the establishment of host-microbe associations; (iii) host mate choice did not itself lead to reproductive isolation, but could reinforce it; (iv) changes in host fitness due to host-microbe associations had a minimal impact upon the formation of co-associations. When we introduced a second population, into which host-microbe carriers could disperse but in which environmental acquisition did not occur, highly efficient VT was required for host-microbe co-associations to persist. Our study reveals that transmission mode is of key importance in establishing host-microbe associations.

evolutionary biology↗

Transgenerational fitness effects of lifespan extension by dietary restriction in Caenorhabditis elegans

Dietary restriction increases lifespan in a broad variety of organisms and improves health in humans. However, long-term transgenerational consequences of dietary interventions are poorly understood. Here we investigated the effect of dietary restriction by temporary fasting (TF) on mortality risk, age-specific reproduction and fitness across three generations of descendants in C. elegans. We show that while TF robustly reduces mortality risk and improves late-life reproduction in the parental generation (P0), it has a wide range of both positive and deleterious effects on future generations (F1-F3). Remarkably, great-grandparental exposure to TF in early-life reduces fitness and increases mortality risk of F3 descendants to such an extent that TF no longer promotes a lifespan extension. These findings reveal that transgenerational trade-offs accompany the instant benefits of dietary restriction underscoring the need to consider fitness of future generations in pursuit of healthy ageing.

evolutionary biology↗

Ataxin-3 links NOD2 and TLR2 mediated innate immune sensing and metabolism in myeloid cells

The interplay between NOD2 and TLR2 following recognition of components of the bacterial cell wall peptidoglycan is well established, however their role in redirecting metabolic pathways in myeloid cells to degrade pathogens and mount antigen presentation remains unclear. We show NOD2 and TLR2 mediate phosphorylation of the deubiquitinase ataxin-3 via RIPK2 and TBK1. In myeloid cells ataxin-3 associates with the mitochondrial cristae protein MIC60, and is required for oxidative phosphorylation. Depletion of ataxin-3 leads to impaired induction of mitochondrial reactive oxygen species (mROS) and defective bacterial killing. A mass spectrometry analysis of NOD2/TLR2 triggered ataxin-3 deubiquitination targets revealed immunometabolic regulators, including HIF-1 and LAMTOR1 that may contribute to these effects. Thus, we define how ataxin-3 plays an essential role in NOD2 and TLR2 sensing and effector functions in myeloid cells.\n\nSignificance StatementIn recent years it has become clear that cross-talk between metabolic and immune pathways is central to the regulation of host defence. This interplay appears of particular importance in myeloid cells including dendritic cells and macrophages, but it is unclear how two of their key bacterial sensors NOD2 and TLR2 influence metabolism. Here, we define how NOD2/TLR2 signal in myeloid cells to drive optimal mitochondrial functioning required for bacterial destruction. We uncover a new role for Ataxin-3, a deubiquitinase required for non-selective autophagy, in this pathway. We provide a non-biased analysis of Ataxin-3 targets generating evidence for a role in deubiquitination of metabolic mediators during myeloid cell differentiation that will provide an important basis for further study.

immunology↗

NOD2 and TLR2 Signal via TBK1 and PI31 to Direct Cross-presentation and CD8 T Cell Responses

NOD2 and TLR2 recognize components of bacterial cell wall peptidoglycan and direct defense against enteric pathogens. CD8+ T cells are important for immunity to such pathogens but how NOD2 and TLR2 induce antigen specific CD8+ T cell responses is unknown. Here, we define how these pattern recognition receptors (PRRs) signal in primary dendritic cells (DCs) to influence MHC class I antigen presentation. We show NOD2 and TLR2 phosphorylate PI31 via TBK1 following activation in DCs. PI31 interacts with TBK1 and Sec16A at endoplasmic reticulum exit sites (ERES), which positively regulates MHC class I peptide loading and immunoproteasome stability. Following NOD2 and TLR2 stimulation, depletion of PI31 or inhibition of TBK1 activity in vivo impairs DC cross-presentation and CD8+ T cell activation. DCs from Crohns patients expressing NOD2 polymorphisms show dysregulated cross-presentation and CD8+ T cell responses. Our findings reveal unidentified mechanisms that underlie CD8+ T cell responses to bacteria in health and in Crohns.

immunology↗

Response to a Synthetic Pheromone Source by OX4319L, a Self-Limiting Diamondback Moth (Lepidoptera: Plutellidae) Strain, and Field Dispersal Characteristics of Its Progenitor Strain

The Diamondback Moth, Plutella xylostella (L.) (Lepidoptera: Plutellidae), is a global pest that infests vegetable and field crops within the Brassica family. A genetically engineered strain of P. xylostella, OX4319L, carrying a self-limiting gene, has shown potential for managing P. xylostella populations, using sustained releases of OX4319L male moths. In order for such a strain to provide control, the transgenic individuals must exhibit attraction to female P. xylostella sex pheromone and adequate dispersal in the field. In this study, we tested these key traits. First, we compared the responses of the OX4319L male moths to a synthetic female sex pheromone source in wind tunnel trials to those of males from three other strains. We found that OX4319L males responded comparably to strains of non-engineered males, with all males flying upwind towards the pheromone source. Second, we used mark-release-recapture studies of a wildtype P. xylostella strain, from which the OX4319L strain was originally developed, to assess dispersal under field conditions. Released males were recaptured using both pheromone-baited and passive traps within a 2.83 ha circular cabbage field, with a recapture rate of 7.93%. Males were recaptured up to the boundary of the field at 95 m from the central release point. The median dispersal of males was 14 m. These results showed the progenitor strain of OX4319L retained its ability to disperse within a host field. The results of these experiments are discussed in relation to the potential for the effective use of engineered male-selecting P. xylostella strains under field conditions.

zoology↗

Mate choice and gene expression signatures associated with nutritional adaptation in the medfly (Ceratitis capitata)

Evolutionary responses to nutrition are key to understanding host shifts and the potential for reproductive isolation. Previously, experimental evolution was used to describe responses of the medfly (Ceratitis capitata) to divergent larval diets. Within 30 generations there was divergence in larval development time, egg to adult survival and adaptation in adult body size. In this study, the gene expression signatures associated with these changes were examined, using mRNA-seq on males following 60 generations of nutritional selection. Variation in gene expression was also validated using qRT-PCR. The results showed observed an over-representation of differential expression in metabolism, oxidative phosphorylation and proteolysis genes. In addition, at generations 60 and 90, we tested whether these evolved patterns (differences in gene expression) were associated with mate choice. We found evidence for assortative mating by diet at generation 60, but not in mating tests within and between replicate lines at generation 90. Hence, there was no consistent evidence for assortative mating by diet, which emphasises the importance of replicate tests of evolutionary responses over time. Overall, the study provides the first genome-wide survey of the putative mechanisms underpinning evolved responses to nutritional adaptation.

evolutionary biology↗

Vertically transmitted rhabdoviruses are found across three insect families and have dynamic interactions with their hosts

A small number of free-living viruses have been found to be obligately vertically transmitted, but it remains uncertain how widespread vertically transmitted viruses are and how quickly they can spread through host populations. Recent metagenomic studies have found several insects to be infected with sigma viruses (Rhabdoviridae). Here, we report that sigma viruses that infect Mediterranean fruit flies (Ceratitis capitata), Drosophila immigrans, and speckled wood butterflies (Pararge aegeria) are all vertically transmitted. We find patterns of vertical transmission that are consistent with those seen in Drosophila sigma viruses, with high rates of maternal transmission, and lower rates of paternal transmission. This mode of transmission allows them to spread rapidly in populations, and using viral sequence data we found the viruses in D. immigrans and C. capitata had both recently swept through host populations. The viruses were common in nature, with mean prevalences of 12% in C. capitata, 38% in D. immigrans and 74% in P. aegeria. We conclude that vertically transmitted rhabdoviruses may be widespread in insects, and that these viruses can have dynamic interactions with their hosts.

evolutionary biology↗