The genetic basis and adult reproductive consequences of developmental thermal plasticity

Increasing temperature and thermal variability generate profound selection on populations. Given the fast rate of environmental change, understanding the role of plasticity and genetic adaptation in response to increasing temperatures is critical. This may be especially true for thermal effects on reproductive traits in which thermal fertility limits at high temperatures may be lower than for survival traits. Consequences of changing environments during development on adult phenotypes may be particularly problematic for core traits such as reproduction that begin early in development. Here we examine the consequences of developmental thermal plasticity on subsequent adult reproductive traits and its genetic basis. We used a panel of Drosophila melanogaster (the Drosophila Genetic Reference Panel; DGRP) in which male fertility performance was previously defined as either showing relatively little (status = ‘high’-performing lines) or substantial (‘low’-performing lines) decline when exposed to increasing developmental temperatures. We used a thermal reaction norm approach to quantify variation in the consequences of developmental thermal plasticity on multiple adult reproductive traits, including sex-specific responses, and to identify candidate genes underlying such variation. Developmental thermal stress impacted the means and thermal reaction norms of all reproductive traits except offspring sex ratio. Mating success declined as temperature increased with no difference between high and low lines, whereas increasing temperature resulted in declines for both male and female fertility and productivity but depended on line status. Fertility and offspring number were positively correlated within and between the sexes across lines, but males were more affected than females. We identified 933 SNPs with significant evolved genetic differentiation between high and low lines. In all, 54 of these lie within genomic windows of overall high differentiation, have significant effects of genotype on the male thermal reaction norm for productivity and are associated with 16 genes enriched for phenotypes affecting reproduction, stress responses and autophagy in Drosophila and other organisms. Our results illustrate considerable plasticity in male thermal limits on several reproductive traits following development at high temperature, and we identify differentiated loci with relevant phenotypic effects that may contribute to this population variation. While our work is on a single population, phenotypic results align with an increasing number of studies demonstrating the potential for stronger selection of thermal stress on reproductive traits, particularly in males. Such large fitness costs may have both short- and long-term consequences for the evolution of populations in response to a warming world.info:eu-repo/semantics/publishedVersio

Environmental variation mediates the evolution of anticipatory parental effects

Theory maintains that when future environment is predictable, parents should adjust the phenotype of their offspring to match the anticipated environment. The plausibility of positive anticipatory parental effects is hotly debated and the experimental evidence for the evolution of such effects is currently lacking. We experimentally investigated the evolution of anticipatory maternal effects in a range of environments that differ drastically in how predictable they are. Populations of the nematode Caenorhabditis remanei, adapted to 20°C, were exposed to a novel temperature (25°C) for 30 generations with either positive or zero correlation between parent and offspring environment. We found that populations evolving in novel environments that were predictable across generations evolved a positive anticipatory maternal effect, because they required maternal exposure to 25°C to achieve maximum reproduction in that temperature. In contrast, populations evolving under zero environmental correlation had lost this anticipatory maternal effect. Similar but weaker patterns were found if instead rate-sensitive population growth was used as a fitness measure. These findings demonstrate that anticipatory parental effects evolve in response to environmental change so that ill-fitting parental effects can be rapidly lost. Evolution of positive anticipatory parental effects can aid population viability in rapidly changing but predictable environments

Age-specific trade-offs in life-history evolution

Trade-offs prevent selection from driving all fitness-enhancing traits towards values that would maximize fitness. Life-history trade-offs, such as the one between survival and reproduction are well-studied, yet trade-offs can also involve behavioural or cognitive traits. Because males and females have different routes to successful reproduction, the optimal resolution of life-history trade-offs can differ between the sexes. However, shared genome can constrain the evolution of sex-specific adaptations. In this thesis, I explore the links between sex-specific life histories, cognition and behaviour. I start by linking sex differences in life histories to sex differences in learning performance in the outcrossing nematode Caenorhabditis remanei (Paper I). I report that age-related learning differs between the sexes and that it corresponds to sexual dimorphism in life history. Then, I use experimental evolution to select for learning performance to study the patterns of genetic correlations between learning and life-history traits in both sexes (Paper II). The results demonstrate the correlated evolution of sexual dimorphism in life history indicating sex-specific fitness costs and benefits of learning. In Paper III I use the fruit fly Drosophila melanogaster to ask about the extent to which cognitive and demographic aging are independent. The results reveal that selection for late-life reproduction alone bears no effect on late-life learning and that joint selection on late-life learning and reproduction does not yield lifespan benefits. The selection might have affected, however, female age-specific reproductive effort. Motivated by the questions on aging I proceed to ask why a potent lifespan extending drug – rapamycin affects sexes differently (Paper IV). I take a closer look at the trade-off between growth, lifespan and reproduction and propose that the sex experiencing a stronger relationship between size and fitness pays a higher cost of lifespan extension. Finally, I focus on another sex-specific trait – dispersal (Paper V). I conduct experimental evolution to uncover a negative genetic correlation between dispersal and reproduction and show sex-specific genetic variation for dispersal. In summary, my thesis unravels the complex pattern of interdependence between life-history, behavioural and cognitive traits, where sex emerges as an important factor that can maintain genetic variation for trade-offs

Data from: Experimental evolution of slowed cognitive aging in Drosophila melanogaster

Reproductive output and cognitive performance decline in parallel during aging, but it is unknown whether this reflects a shared genetic architecture or merely the declining force of natural selection acting independently on both traits. We used experimental evolution in Drosophila melanogaster to test for the presence of genetic variation for slowed cognitive aging, and assess its independence from that responsible for other traits’ decline with age. Replicate experimental populations experienced either joint selection on learning and reproduction at old age (Old+Learning), selection on late-life reproduction alone (Old), or a standard two-week culture regime (Young). Within 20 generations, the Old+Learning populations evolved a slower decline in learning with age than both the Old and Young populations, revealing genetic variation for cognitive aging. We found little evidence for a genetic correlation between cognitive and demographic aging: although the Old+Learning populations tended to show higher late-life fecundity than Old populations, they did not live longer. Likewise, selection for late reproduction alone did not result in improved late-life learning. Our results demonstrate that Drosophila harbor genetic variation for cognitive aging that is largely independent from genetic variation for demographic aging and suggest that these two aspects of aging may not necessarily follow the same trajectories

Experimental evolution of slowed cognitive aging in Drosophila melanogaster

Reproductive output and cognitive performance decline in parallel during aging, but it is unknown whether this reflects a shared genetic architecture or merely the declining force of natural selection acting independently on both traits. We used experimental evolution in Drosophila melanogaster to test for the presence of genetic variation for slowed cognitive aging, and assess its independence from that responsible for other traits' decline with age. Replicate experimental populations experienced either joint selection on learning and reproduction at old age (Old + Learning), selection on late-life reproduction alone (Old), or a standard two-week culture regime (Young). Within 20 generations, the Old + Learning populations evolved a slower decline in learning with age than both the Old and Young populations, revealing genetic variation for cognitive aging. We found little evidence for a genetic correlation between cognitive and demographic aging: although the Old + Learning populations tended to show higher late-life fecundity than Old populations, they did not live longer. Likewise, selection for late reproduction alone did not result in improved late-life learning. Our results demonstrate that Drosophila harbor genetic variation for cognitive aging that is largely independent from genetic variation for demographic aging and suggest that these two aspects of aging may not necessarily follow the same trajectories

Full data

Data for learning assays (Experiment 1 and 2), reproductive, lifespan and locomotory activity assays

Total reproduction and lambda - males

Total reproduction and lambda for males. Note that this is based upon the subset of times measured

Slow development as an evolutionary cost of long life

1. Life-history theory predicts a trade-off between early-life fitness and life span. While the focus traditionally has been on the fecundity-life span trade-off, there are strong reasons to expect trade-offs with growth rate and/or development time.  2. We investigated the roles of growth rate and development time in the evolution of life span in two independent selection experiments in the outcrossing nematode Caenorhabditis remanei.  3. First, we found that selection under heat-shock leads to the evolution of increased life span without fecundity costs, but at the cost of slower development.  4. Thereafter, the putative evolutionary links between development time, growth rate, fecundity, heat-shock resistance and life span were independently assessed in the second experiment by directly selecting for fast or slow development. This experiment confirmed our initial findings, since selection for slow development resulted in the evolution of long life span and increased heat-shock resistance. 5. Because there were no consistent trade-offs with growth rate or fecundity, our results highlight the key role of development rate - differentiation of the somatic cells per unit of time - in the evolution of life span.  6. Since development time is under strong selection in nature, reduced somatic maintenance resulting in shorter life span may be a widespread cost of rapid development