Rapid turnover of a pea aphid superclone mediated by thermal endurance in central Chile.

Global change drivers are imposing novel conditions on Earth's ecosystems at an unprecedented rate. Among them, biological invasions and climate change are of critical concern. It is generally thought that strictly asexual populations will be more susceptible to rapid environmental alterations due to their lack of genetic variability and, thus, of adaptive responses. In this study, we evaluated the persistence of a widely distributed asexual lineage of the alfalfa race of the pea aphid, Acyrthosiphon pisum, along a latitudinal transect of approximately 600 km in central Chile after facing environmental change for a decade. Based on microsatellite markers, we found an almost total replacement of the original aphid superclone by a new variant. Considering the unprecedented warming that this region has experienced in recent years, we experimentally evaluated the reproductive performance of these two A. pisum lineages at different thermal regimes. The new variant exhibits higher rates of population increase at warmer temperatures, and computer simulations employing a representative temperature dataset suggest that it might competitively displace the original superclone. These results support the idea of a superclone turnover mediated by differential reproductive performance under changing temperatures.

Phenotypic specialization of the pea aphid in its southern limit of distribution.

The success of biological invasions ultimately relies on phenotypic traits of the invasive species. Aphids, which include many important pests worldwide, may have been successful invading new environments partly because they can maximize reproductive output by becoming parthenogenetic and losing the sexual phase of their reproductive cycle. However, invasive populations of aphids invading wide ranges can face contrasting environmental conditions and requiring different phenotypic strategies. Besides transitions in their reproductive cycle, it is only partially known which phenotypic traits might be associated to the invasion success of aphid populations in extended novel ranges. Here, we used four genotypes of the pea aphid Acyrthosiphon pisum from two localities in Chile to test for phenotypic specialization that might explain their establishment and spread in habitats exhibiting contrasting environmental conditions. We show that lineages living at a higher latitude with low temperatures show, in addition to facultative sexual reproduction, smaller body sizes, lower metabolic rates and a higher tolerance to the cold than the obligate asexual lineages living in a mild weather, at the expense of fecundity. Conversely, at higher temperatures only asexual lineages were found, which exhibit larger body sizes, higher reproductive outputs and consequently enhanced demographic ability. As a result, in conjunction with the reproductive mode, lineage specialization in physiological and life-history traits could be taken into account as an important strategy for populations of pea aphid to effectively invade extended novel ranges comprising different climatic conditions.

Thermal effects vary predictably across levels of organization: empirical results and theoretical basis.

Thermal performance curves have provided a common framework to study the impact of temperature in biological systems. However, few generalities have emerged to date. Here, we combine an experimental approach with theoretical analyses to demonstrate that performance curves are expected to vary predictably with the levels of biological organization. We measured rates of enzymatic reactions, organismal performance and population viability in Drosophila acclimated to different thermal conditions and show that performance curves become narrower with thermal optima shifting towards lower temperatures at higher levels or organization. We then explain these results on theoretical grounds, showing that this pattern reflects the cumulative impact of asymmetric thermal effects that piles up with complexity. These results and the proposed framework are important to understand how organisms, populations and ecological communities might respond to changing thermal conditions.

Latitudinal trend in the reproductive mode of the pea aphid Acyrthosiphon pisum invading a wide climatic range.

The maintenance of sexuality is a puzzling phenomenon in evolutionary biology. Many universal hypotheses have been proposed to explain the prevalence of sex despite its costs, but it has been hypothesized that sex could be also retained by lineage-specific mechanisms that would confer some short-term advantage. Aphids are good models to study the maintenance of sex because they exhibit coexistence of both sexual and asexual populations within the same species and because they invade a large variety of ecosystems. Sex in aphids is thought to be maintained because only sexually produced eggs can persist in cold climates, but whether sex is obligate or facultative depending on climatic conditions remains to be elucidated. In this study, we have inferred the reproductive mode of introduced populations of the pea aphid Acyrthosiphon pisum in Chile along a climatic gradient using phenotypic assays and genetic-based criteria to test the ecological short-term advantage of sex in cold environments. Our results showed a latitudinal trend in the reproductive mode of Chilean pea aphid population from obligate parthenogenesis in the north to an intermediate life cycle producing both parthenogenetic and sexual progeny in the southernmost locality, where harsh winters are usual. These findings are congruent with the hypothesis of the ecological short-term advantage of sex in aphids.

Dietary effect on immunological energetics in mice.

Defense against natural aggressors, such as bacterial infections, requires both energy and an immune-cellular response. However, the question as to how these two components are interconnected in small endotherms by means of the host diet remains only poorly understood. Here, we tested in laboratory mice whether dietary proteins and carbohydrates can modulate the interplay between energy expenditure, food intake and the innate and adaptive immune response when confronting a bacterial challenge (Bacillus Calmette-Guérin, BCG). We observed that mice fed with a high protein diet (HP) developed a better immune response associated to increased numbers of circulating monocytes. In addition, HP diet directly influenced the peripheral blood proportions of both T and B lymphocytes even before the BCG challenge. Interestingly, animals that developed this type of immune response after BCG challenge showed an increased rate of metabolism and food consumption before being challenged. Thus, HP diet induced in non-challenged animals a similar energy expenditure and food intake described by BCG-treated mice. These data suggest that a high amount of proteins in diet can modify the energetic and nutrient dynamic in the host causing a better immune reaction against a microbial challenge.

Testing the heat-invariant and cold-variability tolerance hypotheses across geographic gradients.

Changes in temperature across geographic gradients can occur on a wide temporal range, from fluctuations within hours as a result of day-night to those over many years. These events will drive many organisms towards their physiological limits of thermal tolerance. Recently, many reports support a limited scope for adaptive evolutionary responses to high temperatures, meaning a conserved heat tolerance among ectotherms in general. We address this problem and tested the heat and cold tolerance invariant-variant hypotheses in terrestrial isopods. We studied five different populations of Porcellio laevis and three populations of Porcellio scaber, spanning 30° S latitudinal gradient in Chile. The heat tolerance of woodlice was conserved with little variation along latitude and environmental temperatures, but cold tolerance decreases significantly with environmental temperatures and latitudes. Indeed, a significant and negative correlation was observed between cold tolerance and latitude. Also, significant and positive correlations were observed among cold tolerance and environmental temperatures. Conversely, heat tolerance was not significantly correlated with any of the environmental temperatures tested neither with latitude. This macrophysiological pattern indicated that heat and cold-tolerances of species and populations not always change across geographical gradients meaning that thermal tolerance responses to high temperatures may be evolutionary constrained.

Differential responses to thermal variation between fitness metrics.

Temperature is a major factor affecting population abundance and individual performance. Net reproductive rate (R0) and intrinsic rate of increase (r) differ in their response to different temperature regimes, and much of the difference is mediated by generation time (Tg). Here, we evaluate the effects of thermal mean and variability on R0, r and Tg, at four population densities in Drosophila melanogaster. The results show that R0, r and Tg present differential responses to thermal variation. Although temperature effects on R0 and Tg are non-linear, r response was negligible. R0 and Tg comprise a generational time scale, while r is at a chronological time scale. Thus, we argue that individuals growing under different thermal environments perform similarly on a chronological scale, but differently on a generational scale.