Temperature change exerts sex-specific effects on behavioural variation.

Temperature is a key factor mediating organismal fitness and has important consequences for species' ecology. While the mean effects of temperature on behaviour have been well-documented in ectotherms, how temperature alters behavioural variation among and within individuals, and whether this differs between the sexes, remains unclear. Such effects likely have ecological and evolutionary consequences, given that selection acts at the individual level. We investigated the effect of temperature on individual-level behavioural variation and metabolism in adult male and female Drosophila melanogaster (n = 129), by taking repeated measures of locomotor activity and metabolic rate at both a standard temperature (25°C) and a high temperature (28°C). Males were moderately more responsive in their mean activity levels to temperature change when compared to females. However, this was not true for either standard or active metabolic rate, where no sex differences in thermal metabolic plasticity were found. Furthermore, higher temperatures increased both among- and within-individual variation in male, but not female, locomotor activity. Given that behavioural variation can be critical to population persistence, we suggest that future studies test whether sex differences in the amount of behavioural variation expressed in response to temperature change may result in sex-specific vulnerabilities to a warming climate.

Indigenous and introduced Collembola differ in desiccation resistance but not its plasticity in response to temperature.

Biological invasions have significant ecological and economic impacts. Much attention is therefore focussed on predicting establishment and invasion success. Trait-based approaches are showing much promise, but are mostly restricted to investigations of plants. Although the application of these approaches to animals is growing rapidly, it is rare for arthropods and restricted mostly to investigations of thermal tolerance. Here we study the extent to which desiccation tolerance and its phenotypic plasticity differ between introduced (nine species) and indigenous (seven species) Collembola, specifically testing predictions of the 'ideal weed' and 'phenotypic plasticity' hypotheses of invasion biology. We do so on the F2 generation of adults in a full factorial design across two temperatures, to elicit desiccation responses, for the phenotypic plasticity trials. We also determine whether basal desiccation resistance responds to thermal laboratory natural selection. We first show experimentally that acclimation to different temperatures elicits changes to cuticular structure and function that are typically associated with water balance, justifying our experimental approach. Our main findings reveal that basal desiccation resistance differs, on average, between the indigenous and introduced species, but that this difference is weaker at higher temperatures, and is driven by particular taxa, as revealed by phylogenetic generalised least squares approaches. By contrast, the extent or form of phenotypic plasticity does not differ between the two groups, with a 'hotter is better' response being most common. Beneficial acclimation is characteristic of only a single species. Laboratory natural selection had little influence on desiccation resistance over 8-12 generations, suggesting that environmental filtering rather than adaptation to new environments may be an important factor influencing Collembola invasions.

Parthenogenesis without costs in a grasshopper with hybrid origins.

The rarity of parthenogenetic species is typically attributed to the reduced genetic variability that accompanies the absence of sex, yet natural parthenogens can be surprisingly successful. Ecological success is often proposed to derive from hybridization through enhanced genetic diversity from repetitive origins or enhanced phenotypic breadth from heterosis. Here, we tested and rejected both hypotheses in a classic parthenogen, the diploid grasshopper Warramaba virgo. Genetic data revealed a single hybrid mating origin at least 0.25 million years ago, and comparative analyses of 14 physiological and life history traits showed no evidence for altered fitness relative to its sexual progenitors. Our findings imply that the rarity of parthenogenesis is due to constraints on origin rather than to rapid extinction.

Hydrogen-Oxidizing Bacteria Are Abundant in Desert Soils and Strongly Stimulated by Hydration.

How the diverse bacterial communities inhabiting desert soils maintain energy and carbon needs is much debated. Traditionally, most bacteria are thought to persist by using organic carbon synthesized by photoautotrophs following transient hydration events. Recent studies focused on Antarctic desert soils have revealed, however, that some bacteria use atmospheric trace gases, such as hydrogen (H2), to conserve energy and fix carbon independently of photosynthesis. In this study, we investigated whether atmospheric H2 oxidation occurs in four nonpolar desert soils and compared this process to photosynthesis. To do so, we first profiled the distribution, expression, and activities of hydrogenases and photosystems in surface soils collected from the South Australian desert over a simulated hydration-desiccation cycle. Hydrogenase-encoding sequences were abundant in the metagenomes and metatranscriptomes and were detected in actinobacterial, acidobacterial, and cyanobacterial metagenome-assembled genomes. Native dry soil samples mediated H2 oxidation, but rates increased 950-fold following wetting. Oxygenic and anoxygenic phototrophs were also detected in the community but at lower abundances. Hydration significantly stimulated rates of photosynthetic carbon fixation and, to a lesser extent, dark carbon assimilation. Hydrogenase genes were also widespread in samples from three other climatically distinct deserts, the Namib, Gobi, and Mojave, and atmospheric H2 oxidation was also greatly stimulated by hydration at these sites. Together, these findings highlight that H2 is an important, hitherto-overlooked energy source supporting bacterial communities in desert soils. Contrary to our previous hypotheses, however, H2 oxidation occurs simultaneously rather than alternately with photosynthesis in such ecosystems and may even be mediated by some photoautotrophs.IMPORTANCE Desert ecosystems, spanning a third of the earth's surface, harbor remarkably diverse microbial life despite having a low potential for photosynthesis. In this work, we reveal that atmospheric hydrogen serves as a major previously overlooked energy source for a large proportion of desert bacteria. We show that both chemoheterotrophic and photoautotrophic bacteria have the potential to oxidize hydrogen across deserts sampled across four continents. Whereas hydrogen oxidation was slow in native dry deserts, it increased by three orders of magnitude together with photosynthesis following hydration. This study revealed that continual harvesting of atmospheric energy sources may be a major way that desert communities adapt to long periods of water and energy deprivation, with significant ecological and biogeochemical ramifications.

Basal tolerance but not plasticity gives invasive springtails the advantage in an assemblage setting.

As global climates change, alien species are anticipated to have a growing advantage relative to their indigenous counterparts, mediated through consistent trait differences between the groups. These insights have largely been developed based on interspecific comparisons using multiple species examined from different locations. Whether such consistent physiological trait differences are present within assemblages is not well understood, especially for animals. Yet, it is at the assemblage level that interactions play out. Here, we examine whether physiological trait differences observed at the interspecific level are also applicable to assemblages. We focus on the Collembola, an important component of the soil fauna characterized by invasions globally, and five traits related to fitness: critical thermal maximum, minimum and range, desiccation resistance and egg development rate. We test the predictions that the alien component of a local assemblage has greater basal physiological tolerances or higher rates, and more pronounced phenotypic plasticity than the indigenous component. Basal critical thermal maximum, thermal tolerance range, desiccation resistance, optimum temperature for egg development, the rate of development at that optimum and the upper temperature limiting egg hatching success are all significantly higher, on average, for the alien than the indigenous components of the assemblage. Outcomes for critical thermal minimum are variable. No significant differences in phenotypic plasticity exist between the alien and indigenous components of the assemblage. These results are consistent with previous interspecific studies investigating basal thermal tolerance limits and development rates and their phenotypic plasticity, in arthropods, but are inconsistent with results from previous work on desiccation resistance. Thus, for the Collembola, the anticipated advantage of alien over indigenous species under warming and drying is likely to be manifest in local assemblages, globally.

Tracheal branching in ants is area-decreasing, violating a central assumption of network transport models.

The structure of tubular transport networks is thought to underlie much of biological regularity, from individuals to ecosystems. A core assumption of transport network models is either area-preserving or area-increasing branching, such that the summed cross-sectional area of all child branches is equal to or greater than the cross-sectional area of their respective parent branch. For insects, the most diverse group of animals, the assumption of area-preserving branching of tracheae is, however, based on measurements of a single individual and an assumption of gas exchange by diffusion. Here we show that ants exhibit neither area-preserving nor area-increasing branching in their abdominal tracheal systems. We find for 20 species of ants that the sum of child tracheal cross-sectional areas is typically less than that of the parent branch (area-decreasing). The radius, rather than the area, of the parent branch is conserved across the sum of child branches. Interpretation of the tracheal system as one optimized for the release of carbon dioxide, while readily catering to oxygen demand, explains the branching pattern. Our results, together with widespread demonstration that gas exchange in insects includes, and is often dominated by, convection, indicate that for generality, network transport models must include consideration of systems with different architectures.

Sex-specific effects of mitochondrial haplotype on metabolic rate in Drosophila melanogaster support predictions of the Mother's Curse hypothesis.

Evolutionary theory proposes that maternal inheritance of mitochondria will facilitate the accumulation of mitochondrial DNA (mtDNA) mutations that are harmful to males but benign or beneficial to females. Furthermore, mtDNA haplotypes sampled from across a given species distribution are expected to differ in the number and identity of these 'male-harming' mutations they accumulate. Consequently, it is predicted that the genetic variation which delineates distinct mtDNA haplotypes of a given species should confer larger phenotypic effects on males than females (reflecting mtDNA mutations that are male-harming, but female-benign), or sexually antagonistic effects (reflecting mutations that are male-harming, but female-benefitting). These predictions have received support from recent work examining mitochondrial haplotypic effects on adult life-history traits in Drosophila melanogaster. Here, we explore whether similar signatures of male-bias or sexual antagonism extend to a key physiological trait-metabolic rate. We measured the effects of mitochondrial haplotypes on the amount of carbon dioxide produced by individual flies, controlling for mass and activity, across 13 strains of D. melanogaster that differed only in their mtDNA haplotype. The effects of mtDNA haplotype on metabolic rate were larger in males than females. Furthermore, we observed a negative intersexual correlation across the haplotypes for metabolic rate. Finally, we uncovered a male-specific negative correlation, across haplotypes, between metabolic rate and longevity. These results are consistent with the hypothesis that maternal mitochondrial inheritance has led to the accumulation of a sex-specific genetic load within the mitochondrial genome, which affects metabolic rate and that may have consequences for the evolution of sex differences in life history. This article is part of the theme issue 'Linking the mitochondrial genotype to phenotype: a complex endeavour'.

Comparing thermal performance curves across traits: how consistent are they?

Thermal performance curves (TPCs) are intended to approximate the relationship between temperature and fitness, and are commonly integrated into species distributional models for understanding climate change responses. However, TPCs may vary across traits because selection and environmental sensitivity (plasticity) differ across traits or because the timing and duration of the temperature exposure, here termed time scale, may alter trait variation. Yet, the extent to which TPCs vary temporally and across traits is rarely considered in assessments of climate change responses. Using a common garden approach, we estimated TPCs for standard metabolic rate (SMR), and activity in Drosophila melanogaster at three test temperatures (16, 25 and 30°C), using flies from each of six developmental temperatures (16, 18, 20, 25, 28 and 30°C). We examined the effects of time scale of temperature exposure (minutes/hours versus days/weeks) in altering TPC shape and position, and commonly used descriptors of the TPC: thermal optimum (Topt), thermal limits (Tmin and Tmax) and thermal breadth (Tbr). In addition, we collated previously published estimates of TPCs for fecundity and egg-to-adult viability in D. melanogaster We found that the descriptors of the TPCs varied across traits (egg-to-adult viability, SMR, activity and fecundity), but variation in TPCs within these traits was small across studies when measured at the same time scales. The time scale at which traits were measured contributed to greater variation in TPCs than the observed variance across traits, although the relative importance of time scale differed depending on the trait (activity versus fecundity). Variation in the TPC across traits and time scales suggests that TPCs using single traits may not be an accurate predictor of fitness and thermal adaptation across environments.

Can a Terrestrial Ectoparasite Disperse with Its Marine Host?

One of the most extreme examples of parasite adaptation comes from terrestrial ectoparasites exploiting marine hosts. Despite the ubiquity of such ectoparasitism and its ecological and evolutionary importance, investigations of the responses of ectoparasites to conditions encountered on their hosts are rare. In the case of penguins and their ticks, current understanding suggests that ticks freely parasitize their hosts on land but are incapable of surviving extended oceanic journeys. We examined this conjecture by assessing the physiological capacity of little penguin ticks to endure at-sea foraging and dispersal events of their hosts. Survival in penguins ticks was not significantly compromised by exposure to depths commonly associated with host dives (40 and 60 m), repeated seawater exposure relevant to the most common (30 s) and longest (120 s) recorded host dives, or extended (48 h) exposure to seawater. Mean (±SD) closed-phase durations in adult and nymphal ticks exhibiting discontinuous gas exchange ( 339±237 and 240±295 s, respectively) exceeded that of the maximum recorded host dive duration (120 s). Normoxic-anoxic-normoxic respirometry also confirmed spiracle closure. Mean metabolic rates ( 0.354±0.220 and 4.853±4.930 µL/h at 25°C for unfed and fed adult females, respectively) were significantly influenced by temperature; optimal and LT50 temperatures for adult ticks and fed nymphal ticks were typically higher than swimming penguin body temperatures. These findings suggest that marine host dispersal is unlikely to present an insurmountable barrier to long-distance tick dispersal. Such dispersal has important implications for evolutionary theory, conservation, and epidemiology.