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Carazo, P.

Publications and source records attributed to Carazo, P..

7 recordsLinked to original sources

Chilling out or heating up? Thermal plasticity of seminal fluid proteins in Drosophila melanogaster

Seminal fluid proteins (SFPs) play crucial roles in reproduction by shaping female post-mating physiology and behaviour, male sperm competition, and sexual conflict between the sexes. However, we mostly ignore how abiotic ecological factors regulate SFP expression and transfer. Here, we use quantitative proteomics in adult flies from a wild Drosophila melanogaster population to test how exposure to natural temperature variation (20{degrees}C, 24{degrees}C and 28{degrees}C) across two-time scales (48h and 13d), and under either no or high sperm competition risk, interact to shape SFP production and transfer. We show that both production and transfer of SFPs was reduced after long-term (13d) exposure to low (20{degrees}C) and high (28{degrees}C) temperatures, including in key proteins (sex peptide and ovulin networks) mediating female post-copulatory responses, sperm competition and sexual conflict. Our results show that natural temperature fluctuations can have a strong effect on SFP production and transfer, and thus on post-copulatory sexual selection dynamics.

evolutionary biology↗

Age-dependent gut microbiota dynamics and their association with male fitness traits in Drosophila melanogaster

Growing evidence suggests that the gut microbiota plays a key role in shaping life history in a wide range of species, including well-studied model organisms like Drosophila melanogaster. Although recent studies have explored the relationship between gut microbiota and female life history, the link between gut microbiota and male life history remains understudied. In this study, we explored the role of gut microbiota in shaping male life history traits by correlating variation in life history traits across genetically homogeneous isolines with their naturally occurring gut microbiota. Using 22 isolines from the Drosophila melanogaster Genetic Reference Panel (DGRP), we measured lifespan, early/late-life reproduction, and early/late-life physiological performance. We characterized the gut microbiota composition in young (5 days old) and old (26 days old) flies using 16S rDNA sequencing. We observed significant variation in male life history traits across isolines, as well as age-related changes in gut microbiota composition. Using machine learning, we showed that gut microbiota composition could predict the age of the organisms with high accuracy. Associations between gut microbiota and life history traits were notable, particularly involving the Acetobacter genus. In early life, the abundance of Acetobacter ascendens was associated with functional aging, while Acetobacter indonesiensis was linked to reproductive senescence. In late life, higher abundances of A. ascendens and Acetobacter pasteurianus were negatively associated with lifespan. These findings highlight the potential role of gut microbiota, especially the Acetobacter genus, in male fitness and aging.

microbiology↗

Thermal phenotypic plasticity of pre- and post-copulatory male harm buffers sexual conflict in wild Drosophila melanogaster

Strong sexual selection frequently leads to sexual conflict and ensuing male harm, whereby males increase their reproductive success at the expense of harming females. Male harm is a widespread evolutionary phenomenon with a strong bearing on population viability. Thus, understanding how it unfolds in the wild is a current priority. Here, we sampled a wild Drosophila melanogaster population and studied male harm across the normal range of temperatures under which it reproduces optimally in nature by comparing female lifetime reproductive success and underlying male harm mechanisms under monogamy (i.e., low male competition/harm) vs. polyandry (i.e., high male competition/harm). While females had equal lifetime reproductive success across temperatures under monogamy, polyandry resulted in a maximum decrease of female fitness at 24{degrees}C (35%), reducing its impact at both 20{degrees}C (22%), and 28{degrees}C (10%). Furthermore, female fitness components and pre- (i.e., harassment) and post-copulatory (i.e., ejaculate toxicity) mechanisms of male harm were asymmetrically affected by temperature. At 20{degrees}C, male harassment of females was reduced, and polyandry accelerated female actuarial ageing. In contrast, the effect of mating on female receptivity (a component of ejaculate toxicity) was affected at 28{degrees}C, where the mating costs for females decreased and polyandry mostly resulted in accelerated reproductive ageing. We thus show that, across a natural thermal range, sexual conflict processes and their effects on female fitness components are plastic and complex. As a result, the net effect of male harm on overall population viability is likely to be lower than previously surmised. We discuss how such plasticity may affect selection, adaptation and, ultimately, evolutionary rescue under a warming climate.

evolutionary biology↗

Male harm suppresses female fitness to affect the dynamics of adaptation and evolutionary rescue

One of the most pressing questions we face as biologists is to understand how climate change will affect the evolutionary dynamics of natural populations and how these dynamics will in turn affect population recovery. Increasing evidence shows that sexual selection favours population viability and local adaptation. However, sexual selection can also foster sexual conflict and drive the evolution of male harm to females. Male harm is extraordinarily widespread and has the potential to suppress female fitness and compromise population growth, yet we currently ignore its net effects across taxa, or its effects on local adaptation and evolutionary rescue. We conducted a comparative meta-analysis to quantify the impact of male harm on female fitness and found an overall negative effect of male harm on female fitness. Negative effects seem to depend on proxies of sexual selection, increasing in species with larger sexual size dimorphism and strong sperm competition. We then developed theoretical models to explore how male harm affects adaptation and evolutionary rescue. We show that, when sexual conflict depends on local adaptation, population decline is reduced, but at the cost of slowing down genetic adaptation. This trade-off suggests that eco-evolutionary feedbacks on sexual conflict can act like a double-edge sword, reducing extinction risk by buffering the demographic costs of climate change, but delaying genetic adaptation. However, variation in the mating system and male harm type can mitigate this trade-off. Our work shows that male harm has widespread negative effects on female fitness and productivity, identifies potential mechanistic factors underlying variability in such costs across taxa, and underscores the importance of male harm on the demographic and evolutionary processes that impact how species adapt to environmental change. Impact summaryFor species to persist in the face of climate change, adaptation needs to be fast enough to prevent extinction. If population decline is too abrupt, adaptation will be less likely to promote recovery, leading to extinction. Therefore, numerous studies have sought to determine how species can adapt and escape extinction. Sexual selection can promote genetic adaptation, but often has a by-product, sexual conflict, that promotes adaptations beneficial for one sex and detrimental to the other. Such is the case of male adaptations that increase male reproduction by harming females (male harm). Male harm is widespread and has been shown to decrease female and population productivity in some species, facilitating extinction. Furthermore, there is increasing evidence that the degree of male harm to females depends on environmental changes and how well males are adapted to them. However, we ignore how strong the effects of sexual conflict across taxa are, or how ecological feedback on sexual conflict may affect the rate of adaptation and population recovery. Here, we first conducted a meta-analysis to quantify the effect of male harm on female fitness and show, across taxa, that there is an overall negative effect that seems to be dependent on proxies of sexual selection. Then, we used a series of theoretical models to show that, although eco-evolutionary feedback on sexual conflict can limit population decline, this comes at the cost of slowing down the rate of adaptation and population recovery. Our study suggests that understanding how quick environmental changes affect sexual conflict can increase our understanding of how populations adapt and recover in the face of climate change.

evolutionary biology↗

Ageing via sexual perception is a by-product of male adaptive plasticity in Drosophila melanogaster

Sensory perception of environmental cues can dramatically modulate ageing across distant taxa. For example, male Drosophila melanogaster age faster if they perceive female cues but fail to mate (ageing via sexual perception). This finding has been a breakthrough for our understanding of the mechanisms of ageing, yet we ignore how and why such responses have evolved. Here, we used D. melanogaster to ask whether ageing via sexual perception may be a by-product of plastic adaptive responses to female cues, and found that while long-term sexual perception leads to reproductive costs, short-term perception increases male lifetime reproductive success in a competitive environment. Simulations under a wide range of socio-sexual and demographic scenario suggest that such plasticity as a response to sexual perception might be a widespread strategy in nature. Finally, we show that sexual perception can significantly magnify sexual selection (15-27% average increase in the opportunity for selection).

evolutionary biology↗

Genetic sex determination and sex-specific lifespan in tetrapods - evidence of a toxic Y effect

Sex-specific lifespans are ubiquitous across the tree of life and exhibit broad taxonomic patterns that remain a puzzle, such as males living longer than females in birds and vice versa in mammals. The prevailing "unguarded-X" hypothesis (UXh) explains this by differential expression of recessive mutations in the X/Z chromosome of the heterogametic sex (e.g., females in birds and males in mammals), but has only received indirect support to date. An alternative hypothesis is that the accumulation of deleterious mutations and repetitive elements on the Y/W chromosome might lower the survival of the heterogametic sex ("toxic Y" hypothesis). Here, we report lower survival of the heterogametic relative to the homogametic sex across 138 species of birds, mammals, reptiles and amphibians, as expected if sex chromosomes shape sex-specific lifespans. We then analysed bird and mammal karyotypes and found that the relative sizes of the X and Z chromosomes are not associated with sex-specific lifespans, contrary to UXh predictions. In contrast, we found that Y size correlates negatively with male survival in mammals, where toxic Y effects are expected to be particularly strong. This suggests that small Y chromosomes benefit male lifespans. Our results confirm the role of sex chromosomes in explaining sex differences in lifespan, but indicate that, at least in mammals, this is better explained by "toxic Y" rather than UXh effects.

evolutionary biology↗

The ecology of sexual conflict: behaviorally plastic responses to temperature variation in the social environment can drastically modulate male harm to females.

Sexual conflict is a fundamental driver of male/female adaptations, an engine of biodiversity, and a crucial determinant of population viability. For example, sexual conflict frequently leads to behavioural adaptations that allow males to displace their rivals, but in doing so harm those same females they are competing to access. Sexual conflict via male harm hence not only deviates females from their fitness optimum, but can decrease population viability and facilitate extinction. Despite this prominent role, we are far from understanding what factors modulate the intensity of sexual conflict, and particularly the role of ecology in mediating underlying behavioural adaptations. In this study we show that, in Drosophila melanogaster, variations in environmental temperature of {+/-}4[Formula]C (within the natural range in the wild) decrease male harm impact on female fitness by between 45-73%. Rate-sensitive fitness estimates indicate that such modulation results in an average rescue of population productivity of 7% at colder temperatures and 23% at hotter temperatures. Our results: a) show that the thermal ecology of social interactions can drastically modulate male harm via behaviourally plasticity, b) identify a potentially crucial ecological factor to understand how sexual conflict operates in nature, and c) suggest that behaviourally plastic responses can lessen the negative effect of sexual conflict on population viability in the face of rapid environmental temperature changes.

evolutionary biology↗