Rapid growth reduces cold resistance: evidence from latitudinal variation in growth rate, cold resistance and stress proteins

Background

Physiological costs of rapid growth may contribute to the observation that organisms typically grow at submaximal rates. Although, it has been hypothesized that faster growing individuals would do worse in dealing with suboptimal temperatures, this type of cost has never been explored empirically. Furthermore, the mechanistic basis of the physiological costs of rapid growth is largely unexplored.

Methodology/Principal Finding

Larvae of the damselfly Ischnura elegans from two univoltine northern and two multivoltine southern populations were reared at three temperatures and after emergence given a cold shock. Cold resistance, measured by chill coma recovery times in the adult stage, was lower in the southern populations. The faster larval growth rates in the southern populations contributed to this latitudinal pattern in cold resistance. In accordance with their assumed role in cold resistance, Hsp70 levels were lower in the southern populations, and faster growing larvae had lower Hsp70 levels. Yet, individual variation in Hsp70 levels did not explain variation in cold resistance.

Conclusions/Significance

We provide evidence for a novel cost of rapid growth: reduced cold resistance. Our results indicate that the reduced cold resistance in southern populations of animals that change voltinism along the latitudinal gradient may not entirely be explained by thermal selection per se but also by the costs of time constraint-induced higher growth rates. This also illustrates that stressors imposed in the larval stage may carry over and shape fitness in the adult stage and highlights the importance of physiological costs in the evolution of life-histories at macro-scales.     

Chemo-enzymatic preparation of copolymeric polythioesters containing branched-chain thioether groups

Branched-chain copolymeric polythioesters (PTE) were formed in good yield (∼87%) by chemoenzymatic reactions including thiyl radical-induced addition of 1,6-hexanedithiol to the >C=C< double bond of dimethyl 1,18-octadec-9-enedioate and transthioesterification of polyfunctional dimethyl 1,18-octadec-9-enedioate with bifunctional 1,6-hexanedithiol catalyzed by immobilized lipase from Rhizomucor miehei. The reactions were performed in vacuo at 80°C without a solvent. PTE was extracted from the reaction mixture using methyl-t-butylether and precipitated from i-hexane. The polymer structure of the i-hexane-insoluble PTE precipitate was elucidated by GPC/SEC showing an average molecular mass (M _w) of 1,857 Da corresponding to a molecular weight range of up to 24,000 Da and a maximum degree of polymerization of up to 50 monomer units. Chemical derivatization with TMSH demonstrated the formation of up to ∼58 mol% of a branched-chain thio(S)ether, i.e., dimethyl S-9-(6-mercaptohexylthio)-1,18-octadecanedioate, and small proportions (∼8 mol%) of a dimeric disulfide formed therefrom. The chemical structures of various low-molecular weight (<900 Da) reaction products formed by transthioesterification, addition reaction or disulfide formation of the reactants or reaction intermediates, e.g., 1,18-octadec-9-enedioic acid methyl(O)ester 6′-S-mercaptohexyl thio(S)ester, dimethyl S-9-(6-mercaptohexylthio)-1,18-octadecanedioate, were elucidated by GC–MS. Similarly, dimethyl S-9-(6-S-methylthiohexylthio)-1,18-octadecanedioate and dimethyl 11,18,19,26-tetrathia-10,27-di-(7-carboxymethyl-heptyl)hexatriacontane-1,36-dioate were detected in the reaction mixtures after derivatization with trimethylsulfonium hydroxide.     

Center of mass mechanics of chimpanzee bipedal walking

Center of mass (CoM) oscillations were documented for 81 bipedal walking strides of three chimpanzees. Full‐stride ground reaction forces were recorded as well as kinematic data to synchronize force to gait events and to determine speed. Despite being a bent‐hip, bent‐knee (BHBK) gait, chimpanzee walking uses pendulum‐like motion with vertical oscillations of the CoM that are similar in pattern and relative magnitude to those of humans. Maximum height is achieved during single support and minimum height during double support. The mediolateral oscillations of the CoM are more pronounced relative to stature than in human walking when compared at the same Froude speed. Despite the pendular nature of chimpanzee bipedalism, energy recoveries from exchanges of kinetic and potential energies are low on average and highly variable. This variability is probably related to the poor phasic coordination of energy fluctuations in these facultatively bipedal animals. The work on the CoM per unit mass and distance (mechanical cost of transport) is higher than that in humans, but lower than that in bipedally walking monkeys and gibbons. The pronounced side sway is not passive, but constitutes 10% of the total work of lifting and accelerating the CoM. CoM oscillations of bipedally walking chimpanzees are distinctly different from those of BHBK gait of humans with a flat trajectory, but this is often described as “chimpanzee‐like” walking. Human BHBK gait is a poor model for chimpanzee bipedal walking and offers limited insights for reconstructing early hominin gait evolution. Am J Phys Anthropol 156:422–433, 2015. © 2014 Wiley Periodicals, Inc.     

Reinforcing effects of non-pathogenic bacteria and predation risk: from physiology to life history

The important ecological role of predation risk in shaping populations, communities and ecosystems is becoming increasingly clear. In this context, synergistic effects between predation risk and other natural stressors on prey organisms are gaining attention. Although non-pathogenic bacteria can be widespread in aquatic ecosystems, their role in mediating effects of predation risk has been ignored. We here address the hypothesis that non-pathogenic bacteria may reinforce the negative effects of predation risk in larvae of the damselfly Coenagrion puella. We found synergistic effects for all three life history variables studied: mortality increased, growth reductions were magnified and bacterial load was higher when both non-lethal stressors were combined. The combined exposure to the bacterium and predation risk considerably impaired the two key antipredator mechanisms of the damselfly larvae: they no longer reduced their food intake under predation risk and showed a synergistic reduction in escape swimming speed. The reinforcing negative effects on the fitness-related traits could be explained by the observed synergistic effects on food intake, swimming muscle mass, immune function and oxidative damage. These are likely widespread consequences of energetic constraints and increased metabolic rates associated with the fight-or-flight response. We therefore hypothesize that the here documented synergistic interactions with non-pathogenic bacteria may be widespread. Our results highlight the ignored ecological role of non-pathogenic bacteria in reinforcing the negative effects of predation risk on prey organisms.     

Integrating large‐scale geographic patterns in flight morphology,flight characteristics and sexual selection in a range‐expanding damselfly

While geographic trait variation along environmental clines is widespread, associated patterns in sexual selection remain largely unexplored. Geographic patterns in sexual selection may be expected if 1) phenotypes vary geographically and sexual selection is dependent on the local phenotypes in the population, and if 2) sexual selection is influenced by geographically structured environmental conditions. We quantified geographic variation in flight‐related traits and flight performance in mated and unmated males and tested for geographic variation in sexual selection on these traits in the poleward range‐expanding damselfly Coenagrion scitulum across a set of eleven core and edge populations ordered along thermal gradients in the larval and in the adult stage. We found little support for trait differentiation between core and edge populations, instead we found considerable geographic trait variation along the larval and adult thermal gradients. As expected under time constraints, body mass decreased with shorter larval growth seasons. Lower temperatures during the adult flight period were associated with a higher body mass, a higher flight speed and a higher fat content; these traits likely evolved to buffer flight ability at suboptimal temperatures and to optimize starvation resistance. Across the large geographic scale, we found a consistent higher flight duration in mated males. Instead, sexual selection for higher fat content was stronger in populations with lower adult flight temperatures and sexual selection for lower body mass acted only in edge populations. Our results indicate sexual selection on flight performance to be consistent over a large geographic scale and this despite the clear geographic patterns in sexual selection on the underlying morphological traits. Our results highlight that to fully understand the fitness implications of geographically changing trait patterns, researchers should consider the entire phenotype–performance–fitness axis and incorporate effects of geographically structured life‐stage specific environmental conditions on this axis.     

Biogeographical survey identifies consistent alternative physiological optima and a minor role for environmental drivers in maintaining a polymorphism

The contribution of adaptive mechanisms in maintaining genetic polymorphisms is still debated in many systems. To understand the contribution of selective factors in maintaining polymorphism, we investigated large-scale (>1000 km) geographic variation in morph frequencies and fitness-related physiological traits in the damselfly Nehalennia irene. As fitness-related physiological traits, we investigated investment in immune function (phenoloxidase activity), energy storage and fecundity (abdomen protein and lipid content), and flight muscles (thorax protein content). In the first part of the study, our aim was to identify selective agents maintaining the large-scale spatial variation in morph frequencies. Morph frequencies varied considerably among populations, but, in contrast to expectation, in a geographically unstructured way. Furthermore, frequencies co-varied only weakly with the numerous investigated ecological parameters. This suggests that spatial frequency patterns are driven by stochastic processes, or alternatively, are consequence of highly variable and currently unidentified ecological conditions. In line with this, the investigated ecological parameters did not affect the fitness-related physiological traits differently in both morphs. In the second part of the study, we aimed at identifying trade-offs between fitness-related physiological traits that may contribute to the local maintenance of both colour morphs by defining alternative phenotypic optima, and test the spatial consistency of such trade-off patterns. The female morph with higher levels of phenoloxidase activity had a lower thorax protein content, and vice versa, suggesting a trade-off between investments in immune function and in flight muscles. This physiological trade-off was consistent across the geographical scale studied and supports widespread correlational selection, possibly driven by male harassment, favouring alternative trait combinations in both female morphs.     

Life-history evolution when Lestes damselflies invaded vernal ponds

We know little about the macroevolution of life-history traits along environmental gradients, especially with regard to the directionality compared to the ancestral states and the associated costs to other functions. Here we examine how age and size at maturity evolved when Lestes damselflies shifted from their ancestral temporary pond habitat (i.e., ponds that may dry once every decade or so) to extremely ephemeral vernal ponds (ponds that routinely dry completely each year). Larvae of three species were reared from eggs until emergence under different levels of photoperiod and transient starvation stress. Compared to the two temporary-pond Lestes, the phylogenetically derived vernal-pond Lestes dryas developed more rapidly across photoperiod treatments until the final instar, and only expressed plasticity in development time in the final instar under photoperiod levels that simulated a later hatching date. The documented change in development rate can be considered adaptive and underlies the success of the derived species in vernal ponds. Results suggest associated costs of faster development are lower mass at maturity and lower immune function after transient starvation stress. These costs may not only have impeded further evolution of the routine development rate to what is physiologically maximal, but also maintained some degree of plasticity to time constraints when the habitat shift occurred.     

Symmetrical gaits of Cebus apella: implications for the functional significance of diagonal sequence gait in primates

Quadrupedal locomotion of primates is distinguished from the quadrupedalism of many other mammals by several features, including a diagonal sequence (DS) footfall used in symmetrical gaits. This presumably unique feature of primate locomotion has been attributed to an ancestral adaptation for cautious arboreal quadrupedalism on thin, flexible branches. However, the functional significance of DS gait remains largely hypothetical. The study presented here tests hypotheses about the functional significance of DS gait by analyzing the gait mechanics of a primate that alternates between DS and lateral sequence (LS) gaits, Cebus apella. Kinematic and kinetic data were gathered from two subjects as they moved across both terrestrial and simulated arboreal substrates. These data were used to test four hypotheses: (1) locomotion on arboreal supports is associated with increased use of DS gait, (2) DS gait is associated with lower peak vertical substrate reaction forces than LS gait, (3) DS gait is associated with greater forelimb/hind limb differentiation in force magnitudes, and (4) DS gait offers increased stability. Our results indicate that animals preferred DS gait on the arboreal substrate, and LS gait while on the ground. Peak vertical substrate reaction forces showed a tendency to be lower in DS gait, but not consistently so. Pole ("arboreal") forces were lower than ground forces in DS gait, but not in LS gait. The preferred symmetrical gait on both substrates was a grounded run or amble, with the body supported by only one limb throughout most of the stride. During periods of bilateral support, the DS gait had predominantly diagonal support couplets. This benefit for stability on an arboreal substrate is potentially outweighed by overstriding, its associated ipsilateral limb interference in DS gait and hind foot positioning in front of the hand on untested territory. DS gait also did not result in an optimal anchoring position of the hind foot under the center of mass of the body at forelimb touchdown. In sum, the results are mixed regarding the superiority of DS gait in an arboreal setting. Consequently, the notion that DS gait is an ancestral adaptation of primates, conditioned by the selection demands of an arboreal environment, remains largely hypothetical.     

Life history plasticity to combined time and biotic constraints in Lestes damselflies from vernal and temporary ponds

Little is known about the ecological correlates and macro-evolution of life history plasticity to time constraints. Here, we compared age and mass at emergence and their plasticity toward combinations of time constraints (delayed larval development), food level and predation risk (caged dragonfly larvae) by rearing two temporary-pond Lestes damselflies ( L. congener and L. forcipatus ) and the derived vernal-pond L. dryas from the eggs until adult emergence in outdoor tubs. Life history plasticity under time constraints, low food and predation risk was as predicted by optimality models. Delayed larvae in all three species accelerated development and showed a lower fat content and a substantially elevated mortality rate. At low food, all species emerged later at a smaller mass. Also under predation risk adults of all species emerged later, and (at high food) at a smaller mass. Unexpectedly, delayed larvae did not show a smaller life history response to predation risk imposed by dragonfly larvae. Compared to the two temporary-pond Lestes studied, the derived species that invaded more ephemeral vernal ponds showed a faster development rate and a lower deceleration of development to low food. It also showed a lower acceleration of development to time constraints, possibly reflecting that it reached development rates near to its physiological maximum. Unexpectedly, the vernal-pond Lestes did not slow its development less under predation risk. Our results stress the importance of evaluating ecological and evolutionary correlates of life history plasticity under as realistic conditions as possible.     

What causes male‐biased sex ratios in mature damselfly populations?

1. Several hypotheses to account for biased sex ratios in mature insect populations were tested by monitoring two field populations of the damselfly Lestes sponsa and by performing experiments in field cages. The population sex ratios are heavily male biased in this species. 2. The observed sex ratio at emergence was even and both sexes emerged synchronously. Females had longer maturation times but these were insufficient to explain the observed sex ratio shift. 3. Mass increases during maturation were consistently larger in females. In agreement with this, immature females made more flights per unit of time, which should make them more vulnerable to predation, however maturation probabilities were lower in females only in one field cage experiment. This inconsistency may be due to long bad weather conditions. Interestingly, predators reduced mass increase and this reduction was larger in females than in males. 4. Calculations based on the sex specific maturation times show that only slightly lower daily survival probabilities during maturation in females are enough to generate the observed sex ratio shift. 5. Mature survival was higher in males than in females in one field population but not in another, indicating that this cannot be a general mechanism causing the sex ratio. A higher maturation probability in males is therefore the most plausible mechanism causing the sex ratio shift in damselfly populations.