Heat tolerance of marine ectotherms in a warming Antarctica.

Global warming is affecting the Antarctic continent in complex ways. Because Antarctic organisms are specialized to living in the cold, they are vulnerable to increasing temperatures, although quantitative analyses of this issue are currently lacking. Here we compiled a total of 184 estimates of heat tolerance belonging to 39 marine species and quantified how survival is affected concomitantly by the intensity and duration of thermal stress. Species exhibit thermal limits displaced toward colder temperatures, with contrasting strategies between arthropods and fish that exhibit low tolerance to acute heat challenges, and brachiopods, echinoderms, and molluscs that tend to be more sensitive to chronic exposure. These differences might be associated with mobility. A dynamic mortality model suggests that Antarctic organisms already encounter temperatures that might be physiologically stressful and indicate that these ecological communities are indeed vulnerable to ongoing rising temperatures.

El calentamiento global está afectando al continente antártico de formas complejas. Dado que los organismos antárticos están especializados a vivir en el frío, son vulnerables al aumento de las temperaturas, aunque en la actualidad hay carencia de análisis cuantitativos al respecto. Aquí recopilamos un total de 184 estimaciones de tolerancia al calor pertenecientes a 39 especies marinas, y cuantificamos cómo la supervivencia de estos organismos se ve afectada concomitantemente por la intensidad y la duración de un estrés térmico. Efectivamente las especies antárticas muestran límites térmicos desplazados hacia temperaturas más frías, con estrategias contrastadas entre los artrópodos y los peces que muestran una baja tolerancia a los desafíos térmicos agudos, y los braquiópodos, equinodermos y moluscos que tienden a ser más sensibles a la exposición crónica. Estas diferencias podrían estar asociadas con la movilidad. Un modelo dinámico de mortalidad sugiere que los organismos antárticos ya se enfrentan a temperaturas que podrían ser fisiológicamente estresantes e indican que estas comunidades ecológicas son realmente vulnerables al aumento continuo de las temperaturas.

Temperature variability and metabolic adaptation in terrestrial and aquatic ectotherms.

Thermodynamics is a major factor determining rates of energy expenditure, rates of biochemical dynamics, and ultimately the biological and ecological processes linked with resilience to global warming in ectothermic organisms. Nonetheless, whether ectothermic organisms exhibit general adaptive metabolic responses to cope with worldwide variation in thermal conditions has remained as an open question. Here we combine a model comparison approach with a global dataset of standard metabolic rates (SMR), including 1,160 measurements across 788 species of aquatic invertebrates, insects, fishes, amphibians and reptiles, to investigate the association between metabolic rates and environmental temperatures in their respective habitats. Our analyses suggest that variation in SMR after removing allometric and thermodynamic effects is best explained by the temperature range encountered across seasons, which always provided a better fit than the average temperature for the hottest and coldest month and mean annual temperatures. This pattern was consistent across taxonomic groups and robust to sensitivity analyses. Nonetheless, aquatic and terrestrial lineages responded differently to seasonality, with SMR declining - 6.8% °C-1 of thermal range across seasons in aquatic organisms and increasing 2.8% °C-1 in terrestrial organisms. These responses may reflect alternative strategies to mitigate the impact of increments in warmer temperatures on energy expenditure, either by means of metabolic reduction in thermally homogeneous water bodies or effective behavioral thermoregulation to exploit temperature heterogeneity on land.

Evolution of a predator-induced, nonlinear reaction norm.

Inducible, anti-predator traits are a classic example of phenotypic plasticity. Their evolutionary dynamics depend on their genetic basis, the historical pattern of predation risk that populations have experienced and current selection gradients. When populations experience predators with contrasting hunting strategies and size preferences, theory suggests contrasting micro-evolutionary responses to selection. Daphnia pulex is an ideal species to explore the micro-evolutionary response of anti-predator traits because they face heterogeneous predation regimes, sometimes experiencing only invertebrate midge predators and other times experiencing vertebrate fish and invertebrate midge predators. We explored plausible patterns of adaptive evolution of a predator-induced morphological reaction norm. We combined estimates of selection gradients that characterize the various habitats that D. pulex experiences with detail on the quantitative genetic architecture of inducible morphological defences. Our data reveal a fine scale description of daphnid defensive reaction norms, and a strong covariance between the sensitivity to cues and the maximum response to cues. By analysing the response of the reaction norm to plausible, predator-specific selection gradients, we show how in the context of this covariance, micro-evolution may be more uniform than predicted from size-selective predation theory. Our results show how covariance between the sensitivity to cues and the maximum response to cues for morphological defence can shape the evolutionary trajectory of predator-induced defences in D. pulex.

The alignment between phenotypic plasticity, the major axis of genetic variation and the response to selection.

Phenotypic plasticity is the ability of a genotype to produce more than one phenotype in order to match the environment. Recent theory proposes that the major axis of genetic variation in a phenotypically plastic population can align with the direction of selection. Therefore, theory predicts that plasticity directly aids adaptation by increasing genetic variation in the direction favoured by selection and reflected in plasticity. We evaluated this theory in the freshwater crustacean Daphnia pulex, facing predation risk from two contrasting size-selective predators. We estimated plasticity in several life-history traits, the G matrix of these traits, the selection gradients on reproduction and survival, and the predicted responses to selection. Using these data, we tested whether the genetic lines of least resistance and the predicted response to selection aligned with plasticity. We found predator environment-specific G matrices, but shared genetic architecture across environments resulted in more constraint in the G matrix than in the plasticity of the traits, sometimes preventing alignment of the two. However, as the importance of survival selection increased, the difference between environments in their predicted response to selection increased and resulted in closer alignment between the plasticity and the predicted selection response. Therefore, plasticity may indeed aid adaptation to new environments.

Heritability of boldness and aggressiveness in the zebrafish.

Behavioural traits that are consistent over time and in different contexts are often referred to as personality traits. These traits influence fitness because they play a major role in foraging, reproduction and survival, and so it is assumed that they have little or no additive genetic variance and, consequently, low heritability because, theoretically, they are under strong selection. Boldness and aggressiveness are two personality traits that have been shown to affect fitness. By crossing single males to multiple females, we estimated the heritability of boldness and aggressiveness in the zebrafish, Danio rerio. The additive genetic variance was statistically significant for both traits and the heritability estimates (95 % confidence intervals) for boldness and aggressiveness were 0.76 (0.49, 0.90) and 0.36 (0.10, 0.72) respectively. Furthermore, there were significant maternal effects accounting for 18 and 9 % of the proportion of phenotypic variance in boldness and aggressiveness respectively. This study shows that there is a significant level of genetic variation in this population that would allow these traits to evolve in response to selection.

Artificial Light at Night (ALAN) causes size-dependent effects on intertidal fish decision-making.

Artificial Light at Night (ALAN) alters cycles of day and night, potentially modifying species' behavior. We assessed whether exposure to ALAN influences decision-making (directional swimming) in an intertidal rockfish (Girella laevisifrons) from the Southeastern Pacific. Using a Y-maze, we examined if exposure to ALAN or natural day/night conditions for one week affected the number of visits and time spent in three Y-maze compartments: dark and lit arms ("safe" and "risky" conditions, respectively) and a neutral "non-decision" area. The results showed that fish maintained in natural day/night conditions visited and spent more time in the dark arm, regardless of size. Instead, fish exposed to ALAN visited and spent more time in the non-decision area and their response was size-dependent. Hence, prior ALAN exposure seemed to disorient or reduce the ability of rock fish to choose dark conditions, deemed the safest for small fish facing predators or other potential threats.

Phenotypic convergence along a gradient of predation risk.

A long-standing question in ecology is whether phenotypic plasticity, rather than selection per se, is responsible for phenotypic variation among populations. Plasticity can increase or decrease variation, but most previous studies have been limited to single populations, single traits and a small number of environments assessed using univariate reaction norms. Here, examining two genetically distinct populations of Daphnia pulex with different predation histories, we quantified predator-induced plasticity among 11 traits along a fine-scale gradient of predation risk by a predator (Chaoborus) common to both populations. We test the hypothesis that plasticity can be responsible for convergence in phenotypes among different populations by experimentally characterizing multivariate reaction norms with phenotypic trajectory analysis (PTA). Univariate analyses showed that all genotypes increased age and size at maturity, and invested in defensive spikes (neckteeth), but failed to quantitatively describe whole-organism response. In contrast, PTA quantified and qualified the phenotypic strategy the organism mobilized against the selection pressure. We demonstrate, at the whole-organism level, that the two populations occupy different areas of phenotypic space in the absence of predation but converge in phenotypic space as predation threat increases.

Geographical origin determines responses to salinity of Mediterranean caddisflies.

Many freshwater ecosystems worldwide, and particularly Mediterranean ones, show increasing levels of salinity. These changes in water conditions could affect abundance and distribution of inhabiting species as well as the provision of ecosystem services. In this study we conduct laboratory experiments using the macroinvertebrate Smicridea annulicornis as a model organism. Our factorial experiments were designed to evaluate the effects of geographical origin of organisms and salinity levels on survival and behavioral responses of caddisflies. The experimental organisms were captured from rivers belonging to three hydrological basins along a 450 Km latitudinal gradient in the Mediterranean region of Chile. Animals were exposed to three conductivity levels, from 180 to 1400 µS/cm, close to the historical averages of the source rivers. We measured the behavioral responses to experimental stimuli and the survival time. Our results showed that geographical origin shaped the behavioral and survival responses to salinity. In particular, survival and activity decreased more strongly with increasing salinity in organisms coming from more dilute waters. This suggests local adaptation to be determinant for salinity responses in this benthic invertebrate species. In the current scenario of fast temporal and spatial changes in water levels and salt concentration, the conservation of geographic intra-specific variation of aquatic species is crucial for lowering the risk of salinity-driven biodiversity loss.

The role of indirect genetic effects in the evolution of interacting reproductive behaviors in the burying beetle, Nicrophorus vespilloides.

Social interactions can give rise to indirect genetic effects (IGEs), which occur when genes expressed in one individual affect the phenotype of another individual. The evolutionary dynamics of traits can be altered when there are IGEs. Sex often involves indirect effects arising from first-order (current) or second-order (prior) social interactions, yet IGEs are infrequently quantified for reproductive behaviors. Here, we use experimental populations of burying beetles that have experienced bidirectional selection on mating rate to test for social plasticity and IGEs associated with focal males mating with a female either without (first-order effect) or with (second-order effect) prior exposure to a competitor, and resource defense behavior (first-order effect). Additive IGEs were detected for mating rate arising from (first-order) interactions with females. For resource defense behavior, a standard variance partitioning analysis provided no evidence of additive genetic variance-either direct or indirect. However, behavior was predicted by focal size relative to that of the competitor, and size is also heritable. Assuming that behavior is causally dependent on relative size, this implies that both DGEs and IGEs do occur (and may potentially interact). The relative contribution of IGEs may differ among social behaviors related to mating which has consequences for the evolutionary trajectories of multivariate traits.

Selection on an antagonistic behavioral trait can drive rapid genital coevolution in the burying beetle, Nicrophorus vespilloides.

Male and female genital morphology varies widely across many taxa, and even among populations. Disentangling potential sources of selection on genital morphology is problematic because each sex is predicted to respond to adaptations in the other due to reproductive conflicts of interest. To test how variation in this sexual conflict trait relates to variation in genital morphology we used our previously developed artificial selection lines for high and low repeated mating rates. We selected for high and low repeated mating rates using monogamous pairings to eliminate contemporaneous female choice and male-male competition. Male and female genital shape responded rapidly to selection on repeated mating rate. High and low mating rate lines diverged from control lines after only 10 generations of selection. We also detected significant patterns of male and female genital shape coevolution among selection regimes. We argue that because our selection lines differ in sexual conflict, these results support the hypothesis that sexually antagonistic coevolution can drive the rapid divergence of genital morphology. The greatest divergence in morphology corresponded with lines in which the resolution of sexual conflict over mating rate was biased in favor of male interests.

Behavioral plasticity and G × E of reproductive tactics in Nicrophorus vespilloides burying beetles.

Phenotypic plasticity is important in the evolution of traits and facilitates adaptation to rapid environmental changes. However, variation in plasticity at the individual level, and the heritable basis underlying this plasticity is rarely quantified for behavioral traits. Alternative behavioral reproductive tactics are key components of mating systems but are not often considered within a phenotypic plasticity framework (i.e., as reaction norms). Here, using lines artificially selected for repeated mating rate, we test for genetic (G × E) sources of variation in reproductive behavior of male Nicrophorus vespilloides burying beetles (including signaling behavior), as well as the role of individual body size, in responsiveness to changes in social environment. The results show that body size influences the response of individuals' signaling behavior to changes in the social environment. Moreover, there was G × E underlying the responses of males to variation in the quality of social environment experienced (relative size of focal male compared to his rival). This shows that individual variation in plasticity and social sensitivity of signaling behavior can evolve in response to selection on investment in mating behavior, with males selected for high mating investment having greater social sensitivity.

Effects of age and experience on contest behavior in the burying beetle, Nicrophorus vespilloides.

Contest behavior forms an important part of reproductive investment. Life-history theory predicts that as individuals age and their residual reproductive value decreases, they should increase investment in contest behavior. However, other factors such as social experience may also be important in determining age-related variation in contest behavior. To understand how selection acts on contest behavior over an individual's lifetime, it is therefore important to tease apart the effects of age per se from other factors that may vary with age. Here, we independently manipulate male age and social experience to examine their effects on male contest behavior in the burying beetle Nicrophorus vespilloides. We found that social experience, but not age, influenced male contest behavior but that these changes in behavior did not alter contest outcomes. Male size (relative to his opponent) was overwhelmingly the most important factor determining contest outcome. Our results suggest that in systems with high variation in fighting ability among males, there may be little opportunity for selection to act on factors that influence contest outcomes by altering motivation to win.

Can invasions occur without change? A comparison of G-matrices and selection in the peach-potato aphid, Myzus persicae.

Most evolutionary research on biological invasions has focused on changes seen between the native and invaded range for a particular species. However, it is likely that species that live in human-modified habitats in their native range might have evolved specific adaptations to those environments, which increase the likelihood of establishment and spread in similar human-altered environments. From a quantitative genetic perspective, this hypothesis suggests that both native and introduced populations should reside at or near the same adaptive peak. Therefore, we should observe no overall changes in the G (genetic variance-covariance) matrices between native and introduced ranges, and stabilizing selection on fitness-related traits in all populations. We tested these predictions comparing three populations of the worldwide pest Myzus persicae from the Middle East (native range) and the UK and Chile (separately introduced ranges). In general, our results provide mixed support for this idea, but further comparisons of other species are needed. In particular, we found that there has been some limited evolution in the studied traits, with the Middle East population differing from the UK and Chilean populations. This was reflected in the structure of the G-matrices, in which Chile differed from both UK and Middle East populations. Furthermore, the amount of genetic variation was massively reduced in Chile in comparison with UK and Middle East populations. Finally, we found no detectable selection on any trait in the three populations, but clones from the introduced ranges started to reproduce later, were smaller, had smaller offspring, and had lower reproductive fitness than clones from the native range.

The effects of reproductive specialization on energy costs and fitness genetic variances in cyclical and obligate parthenogenetic aphids.

Organisms with coexisting sexual and asexual populations are ideal models for studying the consequences of either reproductive mode on the quantitative genetic architecture of life-history traits. In the aphid Rhopalosiphum padi, lineages differing in their sex investment coexist but all share a common parthenogenetic phase. Here, we studied multiple genotypes of R. padi specialized either for sexual and asexual reproduction and compared their genetic variation in fitness during the parthenogenetic phase. Specifically, we estimated maintenance costs as standard metabolic rate (SMR), together with fitness (measured as the intrinsic rate of increase and the net reproductive rate). We found that genetic variation (in terms of broad-sense heritability) in fitness was higher in asexual genotypes compared with sexual genotypes. Also, we found that asexual genotypes exhibited several positive genetic correlations indicating that body mass, whole-animal SMR, and apterous individuals production are contributing to fitness. Hence, it appears that in asexual genotypes, energy is fully allocated to maximize the production of parthenogenetic individuals, the simplest possible form of aphid repertoire of life-histories strategies.

Maternal effects, maternal body size and offspring energetics: a study in the common woodlouse Porcellio laevis.

What are the consequences of the natural variation in maternal body mass on offspring energetic performance? How are performance traits related to thermal physiology and energetics phenotypically integrated on offspring? To answer these questions, fifty breeding pairs of the common terrestrial isopod Porcellio laevis were set up in the lab. Physiological performance, thermal tolerance and thermal sensitivity were measured in F1 adults. Maternal effects were estimated as: the direct influence of maternal body mass and the variation associated with mothers. Phenotypic integration was evaluated using path analysis. Our results show that: (1) maternal body size affects positively offspring long-term metabolism, (2) maternal variation was significant in many of the physiological traits and (3) there is an intricate set of relationships among traits and importantly, that offspring exhibited compensational strategies among metabolism, thermal sensitivity and thermal tolerance traits. Even if we cannot clearly state whether these maternal influences were because of the genes or the environment that mothers provided and thus no predictions can be done regarding their evolutionary consequences, it seems clear that the role of maternal effects on physiology can no longer be ignored. In this sense, there's a lot to be gained by incorporating explicit experimental protocols to test for maternal effects.

A test of the thermal-stress and the cost-of-burrowing hypotheses among populations of the subterranean rodent Spalacopus cyanus.

Subterranean mammals show lower than-allometrically expected-basal metabolic rates (BMR), and several competing hypotheses were suggested to explain how physical microenvironmental conditions and underground life affect subterranean mammalian energetics. Two of these are the thermal-stress and the cost-of-burrowing hypotheses. The thermal-stress hypothesis posits that a lower mass-independent BMR reduces overheating in burrows where convective and evaporative heat loss is low, whereas the cost-of-burrowing hypothesis states that a lower mass-independent BMR may compensate for the extremely high energy expenditure of digging during foraging activity. In this paper we tested both hypotheses at an intraspecific level. We compared seven populations of the subterranean rodent Spalacopus cyanus or cururo from different geographic localities with contrasting habitat conditions. We measured BMR and digging metabolic rate (DMR) through open flow respirometry. Our results support neither the thermal-stress nor the cost-of-burrowing hypothesis. Cururos from habitats with contrasting climatic and soil conditions exhibited similar BMR and DMR when measured under similar semi-natural conditions. It is possible that S. cyanus originated in Andean locations where it adapted to relatively hard soils. Later, when populations moved into coastal areas characterized by softer soils, they may have retained the original adaptation without further phenotypic changes.

Dietary effects on life history traits in a terrestrial isopod: the importance of evaluating maternal effects and trade-offs.

Studies of life history aim to explain patterns in the evolution of reproductive investment, growth, and survival. Trade-offs between traits are a fundamental component of life history theory. In herbivorous arthropods life history traits are often responsive to variation in numerous environmental factors, especially diet quality. Using three artificial diets under controlled laboratory conditions, we examined changes in life history traits (i.e. growth rate, offspring number, offspring size, incubation period), trade-offs between traits, and maternal effect on the growth rate of offspring, in the common woodlouse (terrestrial isopod), Porcellio laevis. The high protein diet had significant impacts on offspring production, triggering a smaller-sized offspring, and demonstrating a trade-off between these last two traits. The high carbohydrate diet seldom exerted a significant effect on incubation period. The quality of dietary items evidently has important consequences on the life history of the mother and, thus, on offspring growth; the directions of these effects, however, were opposite. Mothers fed diets with high protein concentrations presented significant maternal effects, measured as offspring growth rate during later ontogeny. Our results support the notion that protein, rather than carbohydrate, concentrations in the diet limit herbivorous arthropods, and have significant consequences on life history traits, as was seen for P. laevis. Clearly, the change in phenotypic correlations between incubation period and offspring number from negative to positive is an empirical demonstration of the context dependence of life history trait trade-offs.