Multigenerational exposure to increased temperature reduces metabolic rate but increases boldness in Gambusia affinis

Acute exposure to warming temperatures increases minimum energetic requirements in ectotherms. However, over and within multiple generations, increased temperatures may cause plastic and evolved changes that modify the temperature sensitivity of energy demand and alter individual behaviors. Here, we aimed to test whether populations recently exposed to geothermally elevated temperatures express an altered temperature sensitivity of metabolism and behavior. We expected that long‐term exposure to warming would moderate metabolic rate, reducing the temperature sensitivity of metabolism, with concomitant reductions in boldness and activity. We compared the temperature sensitivity of metabolic rate (acclimation at 20 vs. 30°C) and allometric slopes of routine, standard, and maximum metabolic rates, in addition to boldness and activity behaviors, across eight recently divergent populations of a widespread fish species (Gambusia affinis). Our data reveal that warm‐source populations express a reduced temperature sensitivity of metabolism, with relatively high metabolic rates at cool acclimation temperatures and relatively low metabolic rates at warm acclimation temperatures compared to ambient‐source populations. Allometric scaling of metabolism did not differ with thermal history. Across individuals from all populations combined, higher metabolic rates were associated with higher activity rates at 20°C and bolder behavior at 30°C. However, warm‐source populations displayed relatively bolder behavior at both acclimation temperatures compared to ambient‐source populations, despite their relatively low metabolic rates at warm acclimation temperatures. Overall, our data suggest that in response to warming, multigenerational exposure (e.g., plasticity, adaptation) may not result in trait change directed along a simple “pace‐of‐life syndrome” axis, instead causing relative decreases in metabolism and increases in boldness. Ultimately, our data suggest that multigenerational warming may produce a novel combination of physiological and behavioral traits, with consequences for animal performance in a warming world.     

Female extra‐pair behavior is not associated with reduced paternal care in Thorn‐tailed Rayadito

Extra‐pair behavior is present in 76% of socially monogamous bird species with biparental care. This behavior may produce costs to females related to a reduction in paternal care. We estimated the percentage of extra‐pair offspring and quantified paternal care in 44 nests of Thorn‐tailed Rayadito (Aphrastura spinicauda) to assess whether males reduce their parental care when females obtain extra‐pair fertilizations. We used data from a sub‐Antarctic population of Rayadito located on Navarino Island (55°4′S, 67°40′W), southern Chile. We found no statistical support for a relationship between variation in paternal care and the percentage of extra‐pair offspring. We discuss how the inability of breeding males to assess their genetic paternity and potential restrictions on behavioral flexibility may explain this result. Additionally, if paternal care is subjected to sexual selection, this could limit a facultative response to female extra‐pair behavior by males. Finally, it is possible that a reduction in paternal care might not have evolved in this particular locality given the low frequency of extra‐pair paternity in our study population.     

Life‐history attributes of Arctic‐breeding birds drive uneven responses to environmental variability across different phases of the reproductive cycle

Animals exhibit varied life‐history traits that reflect adaptive responses to their environments. For Arctic‐breeding birds, traits related to diet, egg nutrient allocation, clutch size, and chick growth are predicted to be under increasing selection pressure due to rapid climate change and increasing environmental variability across high‐latitude regions. We compared four migratory birds (black brant [Branta bernicla nigricans], lesser snow geese [Chen caerulescens caerulescens], semipalmated sandpipers [Calidris pusilla], and Lapland longspurs [Calcarius lapponicus]) with varied life histories at an Arctic site in Alaska, USA, to understand how life‐history traits help moderate environmental variability across different phases of the reproductive cycle. We monitored aspects of reproductive performance related to the timing of breeding, reproductive investment, and chick growth from 2011 to 2018. In response to early snowmelt and warm temperatures, semipalmated sandpipers advanced their site arrival and bred in higher numbers, while brant and snow geese increased clutch sizes; all four species advanced their nest initiation dates. During chick rearing, longspur nestlings were relatively resilient to environmental variation, whereas warmer temperatures increased the growth rates of sandpiper chicks but reduced growth rates of snow goose goslings. These responses generally aligned with traits along the capital‐income spectrum of nutrient acquisition and altricial–precocial modes of chick growth. Under a warming climate, the ability to mobilize endogenous reserves likely provides geese with relative flexibility to adjust the timing of breeding and the size of clutches. Higher temperatures, however, may negatively affect the quality of herbaceous foods and slow gosling growth. Species may possess traits that are beneficial during one phase of the reproductive cycle and others that may be detrimental at another phase, uneven responses that may be amplified with future climate warming. These results underscore the need to consider multiple phases of the reproductive cycle when assessing the effects of environmental variability on Arctic‐breeding birds.     

Adaptive co‐evolution of mitochondria and the Y‐chromosome: A resolution to conflict between evolutionary opponents

In most species with motile sperm, male fertility depends upon genes located on the Y‐chromosome and in the mitochondrial genome. Coordinated adaptive evolution for the function of male fertility between genes on the Y and the mitochondrion is hampered by their uniparental inheritance in opposing sexes: The Y‐chromosome is inherited uniparentally, father to son, and the mitochondrion is inherited maternally, mother to offspring. Preserving male fertility is problematic, because maternal inheritance permits mitochondrial mutations advantageous to females, but deleterious to male fertility, to accumulate in a population. Although uniparental inheritance with sex‐restricted adaptation also affects genes on the Y‐chromosome, females lack a Y‐chromosome and escape the potential maladaptive consequences of male‐limited selection. Evolutionary models have shown that mitochondrial mutations deleterious to male fertility can be countered by compensatory evolution of Y‐linked mutations that restore it. However, direct adaptive coevolution of Y‐ and mitochondrial gene combinations has not yet been mathematically characterized. We use population genetic models to show that adaptive coevolution of Y and mitochondrial genes are possible when Y‐mt gene combinations have positive effects on male fertility and populations are inbred.     

Plastic adjustments of biparental care behavior across embryonic development under elevated temperature in a marine ectotherm

Phenotypic plasticity in parental care investment allows organisms to promptly respond to rapid environmental changes by potentially benefiting offspring survival and thus parental fitness. To date, a knowledge gap exists on whether plasticity in parental care behaviors can mediate responses to climate change in marine ectotherms. Here, we assessed the plasticity of parental care investment under elevated temperatures in a gonochoric marine annelid with biparental care, Ophryotrocha labronica, and investigated its role in maintaining the reproductive success of this species in a warming ocean. We measured the time individuals spent carrying out parental care activities across three phases of embryonic development, as well as the hatching success of the offspring as a proxy for reproductive success, at control (24℃) and elevated (27℃) temperature conditions. Under elevated temperature, we observed: (a) a significant decrease in total parental care activity, underpinned by a decreased in male and simultaneous parental care activity, in the late stage of embryonic development; and (b) a reduction in hatching success that was however not significantly related to changes in parental care activity levels. These findings, along with the observed unaltered somatic growth of parents and decreased brood size, suggest that potential cost‐benefit trade‐offs between offspring survival (i.e., immediate fitness) and parents'' somatic condition (i.e., longer‐term fitness potential) may occur under ongoing ocean warming. Finally, our results suggest that plasticity in parental care behavior is a mechanism able to partially mitigate the negative effects of temperature‐dependent impacts.     

Shielded environments reduce stress in alien Asteraceae species during hot and dry summers along urban‐to‐rural gradients

Urban environments often host a greater abundance and diversity of alien plant species than rural areas. This is frequently linked to higher disturbance and propagule pressure, but could also be related to the additional establishment of species from warmer native ranges in cities, facilitated by the latter''s higher air temperatures and drier soils. A hitherto unresolved question is how stressful the urban environments become during climate extremes such as heatwaves and droughts. Do such episodes still favor alien plant species, or set them back? We used in situ measured phenotypic leaf and development trait responses of the six most widespread alien Asteraceae species from various native climates along Belgian urban‐to‐rural gradients, measured during two unusually warm and dry summers. Urbanization was characterized by three factors: the percentage of artificially sealed surfaces (urbanity, measured at three spatial scales from in situ to satellite‐based), the vegetation cover and the sky view factor (SVF, fraction of the hemisphere not blocked by buildings or vegetation). Across species, either from colder or warmer native climates, we found a predominant protective effect of shielded environments that block solar radiation (low SVF) along the entire urban‐to‐rural gradient. Such environments induced lower leaf anthocyanins and flavonols indices, indicating heat stress mitigation. Shielded environments also increased specific leaf area (SLA), a typical shade response. We found that vegetated areas had a secondary importance, increasing the chlorophyll content and decreasing the flavonols index, but these effects were not consistent across species. Finally, urbanity at the organism spatial scale decreased plant height, while broader‐scale urbanity had no significant influence. Our results suggest that sealed surfaces constrain alien Asteraceae during unusually warm and dry summers, while shielded environments protect them, possibly canceling out the lack of light. These findings shed new light on alien plant species success along urban‐to‐rural gradients in a changing climate.     

Considering sampling bias in close‐kin mark–recapture abundance estimates of Atlantic salmon

Genetic methods for the estimation of population size can be powerful alternatives to conventional methods. Close‐kin mark–recapture (CKMR) is based on the principles of conventional mark–recapture, but instead of being physically marked, individuals are marked through their close kin. The aim of this study was to evaluate the potential of CKMR for the estimation of spawner abundance in Atlantic salmon and how age, sex, spatial, and temporal sampling bias may affect CKMR estimates. Spawner abundance in a wild population was estimated from genetic samples of adults returning in 2018 and of their potential offspring collected in 2019. Adult samples were obtained in two ways. First, adults were sampled and released alive in the breeding habitat during spawning surveys. Second, genetic samples were collected from out‐migrating smolts PIT‐tagged in 2017 and registered when returning as adults in 2018. CKMR estimates based on adult samples collected during spawning surveys were somewhat higher than conventional counts. Uncertainty was small (CV < 0.15), due to the detection of a high number of parent–offspring pairs. Sampling of adults was age‐ and size‐biased and correction for those biases resulted in moderate changes in the CKMR estimate. Juvenile dispersal was limited, but spatially balanced sampling of adults rendered CKMR estimates robust to spatially biased sampling of juveniles. CKMR estimates based on returning PIT‐tagged adults were approximately twice as high as estimates based on samples collected during spawning surveys. We suggest that estimates based on PIT‐tagged fish reflect the total abundance of adults entering the river, while estimates based on samples collected during spawning surveys reflect the abundance of adults present in the breeding habitat at the time of spawning. Our study showed that CKMR can be used to estimate spawner abundance in Atlantic salmon, with a moderate sampling effort, but a carefully designed sampling regime is required.     

Greater sage‐grouse respond positively to intensive post‐fire restoration treatments

Habitat loss is the most prevalent threat to biodiversity in North America. One of the most threatened landscapes in the United States is the sagebrush (Artemisia spp.) ecosystem, much of which has been fragmented or converted to non‐native grasslands via the cheatgrass‐fire cycle. Like many sagebrush obligates, greater sage‐grouse (Centrocercus urophasianus) depend upon sagebrush for food and cover and are affected by changes to this ecosystem. We investigated habitat selection by 28 male greater sage‐grouse during each of 3 years after a 113,000‐ha wildfire in a sagebrush steppe ecosystem in Idaho and Oregon. During the study period, seeding and herbicide treatments were applied for habitat restoration. We evaluated sage‐grouse responses to vegetation and post‐fire restoration treatments. Throughout the 3 years post‐fire, sage‐grouse avoided areas with high exotic annual grass cover but selected strongly for recovering sagebrush and moderately strongly for perennial grasses. By the third year post‐fire, they preferred high‐density sagebrush, especially in winter when sagebrush is the primary component of the sage‐grouse diet. Sage‐grouse preferred forb habitat immediately post‐fire, especially in summer, but this selection preference was less strong in later years. They also selected areas that were intensively treated with herbicide and seeded with sagebrush, grasses, and forbs, although these responses varied with time since treatment. Wildfire can have severe consequences for sagebrush‐obligate species due to loss of large sagebrush plants used for food and for protection from predators and thermal extremes. Our results show that management efforts, including herbicide application and seeding of plants, directed at controlling exotic annual grasses after a wildfire can positively affect habitat selection by sage‐grouse.     

A Single Hot Event Stimulates Adult Performance but Reduces Egg Survival in the Oriental Fruit Moth,Grapholitha molesta

Climate warming is expected to increase the exposure of insects to hot events (involving a few hours at extreme high temperatures). These events are unlikely to cause widespread mortality but may modify population dynamics via impacting life history traits such as adult fecundity and egg hatching. These effects and their potential impact on population predictions are still largely unknown. In this study, we simulated a single hot event (maximum of 38°C lasting for 4 h) of a magnitude increasingly found under field conditions and examined its effect in the oriental fruit moth, Grapholitha molesta. This hot event had no impact on the survival of G. molesta adults, copulation periods or male longevity. However, the event increased female lifespan and the length of the oviposition period, leading to a potential increase in lifetime fecundity and suggesting hormesis. In contrast, exposure of males to this event markedly reduced the net reproductive value. Male heat treatment delayed the onset of oviposition in the females they mated with, as well as causing a decrease in the duration of oviposition period and lifetime fecundity. Both male and female stress also reduced egg hatch. Our findings of hormetic effects on female performance but concurrent detrimental effects on egg hatch suggest that hot events have unpredictable consequences on the population dynamics of this pest species with implications for likely effects associated with climate warming.     

Thermal effects on reptile reproduction: adaptation and phenotypic plasticity in a montane lizard

Interspecific comparisons suggest a strong association between cool climates and viviparity in reptiles. However, intraspecific comparisons, which provide an opportunity to identify causal pathways and to distinguish facultative (phenotypically plastic) effects from canalized (genetically fixed) responses, are lacking. We documented the reproductive traits in an alpine oviparous lizard, and manipulated thermal regimes of gravid females and their eggs to identify proximate causes of life‐history variation. Embryonic development at oviposition was more advanced in eggs laid by females from high‐elevation populations than in eggs produced by females from lower elevations. In the laboratory, experimentally imposed low maternal body temperatures delayed oviposition and resulted in more advanced embryonic development at oviposition. Warm conditions both in utero and in the nest increased hatching success and offspring body size. Our intraspecific comparisons support the hypothesis that viviparity has evolved in cold‐climate squamates because of the direct fitness advantages that warm temperatures provide developing offspring. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 642–655.     

Cap‐independent translation: A shared mechanism for lifespan extension by rapamycin,acarbose, and 17α‐estradiol

We hypothesized that rapamycin (Rapa), acarbose (ACA), which both increase mouse lifespan, and 17α‐estradiol, which increases lifespan in males (17aE2) all share common intracellular signaling pathways with long‐lived Snell dwarf, PAPPA‐KO, and Ghr−/− mice. The long‐lived mutant mice exhibit reduction in mTORC1 activity, declines in cap‐dependent mRNA translation, and increases in cap‐independent translation (CIT). Here, we report that Rapa and ACA prevent age‐related declines in CIT target proteins in both sexes, while 17aE2 has the same effect only in males, suggesting increases in CIT. mTORC1 activity showed the reciprocal pattern, with age‐related increases blocked by Rapa, ACA, and 17aE2 (in males only). METTL3, required for addition of 6‐methyl‐adenosine to mRNA and thus a trigger for CIT, also showed an age‐dependent increase blunted by Rapa, ACA, and 17aE2 (in males). Diminution of mTORC1 activity and increases in CIT‐dependent proteins may represent a shared pathway for both long‐lived‐mutant mice and drug‐induced lifespan extension in mice.     

Turning to the dark side: LED light at night alters the activity and species composition of a foraging bat assemblage in the northeastern United States

Artificial light at night (ALAN) is a rapidly intensifying form of environmental degradation that can impact wildlife by altering light‐mediated physiological processes that control a broad range of behaviors. Although nocturnal animals are most vulnerable, ALAN''s effects on North American bats have been surprisingly understudied. Most of what is known is based on decades‐old observations of bats around street lights with traditional lighting technologies that have been increasingly replaced by energy‐efficient broad‐spectrum lighting, rendering our understanding of the contemporary effects of ALAN on North American bats even less complete. We experimentally tested the effects of broad‐spectrum ALAN on presence/absence, foraging activity, and species composition in a Connecticut, USA bat community by illuminating foraging habitat with light‐emitting diode (LED) floodlights and comparing acoustic recordings between light and dark conditions. Lighting dramatically decreased presence and activity of little brown bats (Myotis lucifugus), which we detected on only 14% of light nights compared with 65% of dark (lights off) and 69% of control (lights removed) nights. Big brown bat (Eptesicus fuscus) activity on light nights averaged only half that of dark and control nights. Lighting did not affect presence/absence of silver‐haired bats (Lasionycteris noctivagans), but decreased their activity. There were no effects on eastern red bats (Lasiurus borealis) or hoary bats (L. cinereus), which have been described previously as light‐tolerant. Aversion to lighting by some species but not others caused a significant shift in community composition, thereby potentially altering competitive balances from natural conditions. Our results demonstrate that only a small degree of ALAN can represent a significant form of habitat degradation for some North American bats, including the endangered little brown bat. Research on the extent to which different lighting technologies, colors, and intensities affect these species is urgently needed and should be a priority in conservation planning for North America''s bats.     

Rabl2 GTP hydrolysis licenses BBSome‐mediated export to fine‐tune ciliary signaling

Cilia of higher animals sense various environmental stimuli. Proper ciliary signaling requires appropriate extent of BBSome‐mediated export of membrane receptors across ciliary barrier transition zone (TZ) through retrograde intraflagellar transport (IFT) machinery. How the barrier passage is controlled, however, remains unknown. Here, we show that small GTPase Rabl2 functions as a molecular switch for the outward TZ passage. Rabl2‐GTP enters cilia by binding to IFT‐B complex. Its GTP hydrolysis enables the outward TZ passage of the BBSome and its cargos with retrograde IFT machinery, whereas its persistent association leads to their shedding from IFT‐B during the passing process and consequently ciliary retention. Rabl2 deficiency or expression of a GTP‐locked mutant impairs the ciliary hedgehog signaling without interfering with ciliation and respectively results in different spectrums of mouse developmental disorders. We propose that the switch role of Rabl2 ensures proper turnover of the BBSome and ciliary membrane receptors to fine‐tune cilia‐dependent signaling for normal embryonic development and organismic homeostasis.     

No evidence for female kin association,indications for extragroup paternity,and sex‐biased dispersal patterns in wild western gorillas

Characterizing animal dispersal patterns and the rational behind individuals’ transfer choices is a long‐standing question of interest in evolutionary biology. In wild western gorillas (Gorilla gorilla), a one‐male polygynous species, previous genetic findings suggested that, when dispersing, females might favor groups with female kin to promote cooperation, resulting in higher‐than‐expected within‐group female relatedness. The extent of male dispersal remains unclear with studies showing conflicting results. To investigate male and female dispersal patterns and extragroup paternity, we analyzed long‐term field observations, including female spatial proximity data, together with genetic data (10 autosomal microsatellites) on individuals from a unique set of four habituated western gorilla groups, and four additional extragroup males (49 individuals in total). The majority of offspring (25 of 27) were sired by the group male. For two offspring, evidence for extragroup paternity was found. Contrarily to previous findings, adult females were not significantly more related within groups than across groups. Consistently, adult female relatedness within groups did not correlate with their spatial proximity inferred from behavioral data. Adult females were similarly related to adult males from their group than from other groups. Using R _ST statistics, we found significant genetic structure and a pattern of isolation by distance, indicating limited dispersal in this species. Comparing relatedness among females and among males revealed that males disperse farer than females, as expected in a polygamous species. Our study on habituated western gorillas shed light on the dispersal dynamics and reproductive behavior of this polygynous species and challenge some of the previous results based on unhabituated groups.     

Food deprivation exposes sex‐specific trade‐offs between stress tolerance and life span in the copepod Tigriopus californicus

Long life is standardly assumed to be associated with high stress tolerance. Previous work shows that the copepod Tigriopus californicus breaks this rule, with longer life span under benign conditions found in males, the sex with lower stress tolerance. Here, we extended this previous work, raising animals from the same families in food‐replete conditions until adulthood and then transferring them to food‐limited conditions until all animals perished. As in previous work, survivorship under food‐replete conditions favored males. However, under food deprivation life span strongly favored females in all crosses. Compared to benign conditions, average life span under nutritional stress was reduced by 47% in males but only 32% in females. Further, the sex‐specific mitonuclear effects previously found under benign conditions were erased under food limited conditions. Results thus demonstrate that sex‐specific life span, including mitonuclear interactions, are highly dependent on nutritional environment.     

Growth hormone receptor gene disruption in mature‐adult mice improves male insulin sensitivity and extends female lifespan

Studies in multiple species indicate that reducing growth hormone (GH) action enhances healthy lifespan. In fact, GH receptor knockout (GHRKO) mice hold the Methuselah prize for the world''s longest‐lived laboratory mouse. We previously demonstrated that GHR ablation starting at puberty (1.5 months), improved insulin sensitivity and female lifespan but results in markedly reduced body size. In this study, we investigated the effects of GHR disruption in mature‐adult mice at 6 months old (6mGHRKO). These mice exhibited GH resistance (reduced IGF‐1 and elevated GH serum levels), increased body adiposity, reduced lean mass, and minimal effects on body length. Importantly, 6mGHRKO males have enhanced insulin sensitivity and reduced neoplasms while females exhibited increased median and maximal lifespan. Furthermore, fasting glucose and oxidative damage was reduced in females compared to males irrespective of Ghr deletion. Overall, disrupted GH action in adult mice resulted in sexual dimorphic effects suggesting that GH reduction at older ages may have gerotherapeutic effects.     

An empirical test of the bet‐hedging polyandry hypothesis: Female red flour beetles avoid extinction via multiple mating

Bet‐hedging via polyandry (spreading the extinction risk of the female''s lineage over multiple males) may explain the evolution of female multiple mating, which is found in a wide range of animal and plant taxa. This hypothesis posits that females can increase their fitness via polyandrous mating when “unsuitable” males (i.e., males causing reproductive failure for various reasons) are frequent in the population and females cannot discriminate such unsuitable mates. Although recent theoretical studies have shown that polyandry can operate as a bet‐hedging strategy, empirical tests are scarce. In the present study, we tested the bet‐hedging polyandry hypothesis by using the red flour beetle Tribolium castaneum. We compared female reproductive success between monandry and polyandry treatments when females mated with males randomly collected from an experimental population, including 20% irradiated (infertile) males. In addition, we evaluated geometric mean fitness across multiple generations as the index of adaptability of bet‐hedging traits. Polyandrous females showed a significantly higher egg hatching rate and higher geometric mean fitness than monandrous females. These results strongly support the bet‐hedging polyandry hypothesis.     

Sex‐specific aging in animals: Perspective and future directions

Sex differences in aging occur in many animal species, and they include sex differences in lifespan, in the onset and progression of age‐associated decline, and in physiological and molecular markers of aging. Sex differences in aging vary greatly across the animal kingdom. For example, there are species with longer‐lived females, species where males live longer, and species lacking sex differences in lifespan. The underlying causes of sex differences in aging remain mostly unknown. Currently, we do not understand the molecular drivers of sex differences in aging, or whether they are related to the accepted hallmarks or pillars of aging or linked to other well‐characterized processes. In particular, understanding the role of sex‐determination mechanisms and sex differences in aging is relatively understudied. Here, we take a comparative, interdisciplinary approach to explore various hypotheses about how sex differences in aging arise. We discuss genomic, morphological, and environmental differences between the sexes and how these relate to sex differences in aging. Finally, we present some suggestions for future research in this area and provide recommendations for promising experimental designs.