Climate change impacts on seabirds and marine mammals: The importance of study duration,thermal tolerance and generation time

Understanding climate change impacts on top predators is fundamental to marine biodiversity conservation, due to their increasingly threatened populations and their importance in marine ecosystems. We conducted a systematic review of the effects of climate change (prolonged, directional change) and climate variability on seabirds and marine mammals. We extracted data from 484 studies (4808 published studies were reviewed), comprising 2215 observations on demography, phenology, distribution, diet, behaviour, body condition and physiology. The likelihood of concluding that climate change had an impact increased with study duration. However, the temporal thresholds for the effects of climate change to be discernibly varied from 10 to 29 years depending on the species, the biological response and the oceanic study region. Species with narrow thermal ranges and relatively long generation times were more often reported to be affected by climate change. This provides an important framework for future assessments, with guidance on response- and region-specific temporal dimensions that need to be considered when reporting effects of climate change. Finally, we found that tropical regions and non-breeding life stages were poorly covered in the literature, a concern that should be addressed to enable a better understanding of the vulnerability of marine predators to climate change.     

Intraspecific variation in seedling drought tolerance and associated traits in a critically endangered,endemic Hawaiian shrub

ABSTRACT

Background

Climates are changing at a rate that exceeds the adaptive capacity of species, especially endangered species. Genetic variation and phenotypic plasticity are important for population persistence, yet few studies have linked traits to seedling performance under drought in endangered species.     

Neurodegeneration of Drosophila drop-dead mutants is associated with hypoxia in the brain

The Drosophila drop-dead (drd) mutant undergoes massive brain degeneration, resulting in sudden death. drd encodes a multi-pass membrane protein possessing nose resistant to fluoxetine (NRF) and putative acyltransferase domains. However, the etiology of brain degeneration that occurs in drd mutant flies is still poorly understood. Herein, we show that drd neurodegeneration may be because of an oxygen deficit in the brain. We found that DRD protein is selectively expressed in cells secreting cuticular and eggshell layers. These layers exhibit blue fluorescence upon UV excitation, which is reduced in drd flies. The drd tracheal air sacs lacking blue fluorescence collapse, which likely contributes to hypoxia. Consistently, genes induced in hypoxia are up-regulated in drd flies. Feeding of anti-reactive oxygen species agents partially rescue the drd from sudden death. We propose that drd flies can provide a non-invasive animal model for hypoxia-induced cell death.     

Seasonal variability in resilience of a coral reef fish to marine heatwaves and hypoxia

Climate change projections indicate more frequent and severe tropical marine heatwaves (MHWs) and accompanying hypoxia year-round. However, most studies have focused on peak summer conditions under the assumption that annual maximum temperatures will induce the greatest physiological consequences. This study challenges this idea by characterizing seasonal MHWs (i.e., mean, maximum, and cumulative intensities, durations, heating rates, and mean annual occurrence) and comparing metabolic traits (i.e., standard metabolic rate (SMR), Q10 of SMR, maximum metabolic rate (MMR), aerobic scope, and critical oxygen tension (P_crit)) of winter- and summer-acclimatized convict tang (Acanthurus triostegus) to the combined effects of MHWs and hypoxia. Fish were exposed to one of six MHW treatments with seasonally varying maximum intensities (winter: 24.5, 26.5, 28.5°C; summer: 28.5, 30.5, 32.5°C), representing past and future MHWs under IPCC projections (i.e., +0, +2, +4°C). Surprisingly, MHW characteristics did not significantly differ between seasons, yet SMR was more sensitive to winter MHWs (mean Q10 = 2.92) than summer MHWs (mean Q10 = 1.81), despite higher absolute summer temperatures. Concurrently, MMR increased similarly among winter +2 and +4°C treatments (i.e., 26.5, 28.5°C) and all summer MHW treatments, suggesting a ceiling for maximal MMR increase. Aerobic scope did not significantly differ between seasons nor among MHW treatments. While mean P_crit did not significantly vary between seasons, warming of +4°C during winter (i.e., 28.5°C) significantly increased P_crit relative to the winter control group. Contrary to the idea of increased sensitivity to MHWs during the warmest time of year, our results reveal heightened sensitivity to the deleterious effects of winter MHWs, and that seasonal acclimatization to warmer summer conditions may bolster metabolic resilience to warming and hypoxia. Consequently, physiological sensitivity to MHWs and hypoxia may extend across larger parts of the year than previously expected, emphasizing the importance of evaluating climate change impacts during cooler seasons when essential fitness-related traits such as reproduction occur in many species.     

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.     

Comparison of variability associated with sample preparation in two-dimensional gel electrophoresis of cardiac tissue.

Variability is a major complicating factor in analysis by two-dimensional gel electrophoresis. Improvements in methodologies have focused on improving individual gel quality rather than reproducibility. We homogenized rat cardiac tissue and rehydrated using a matrix of buffers to determine the optimal sample conditions. Six buffers were used to solubilize the proteins. Solubilized proteins were separated by isoelectric focusing using four buffers. Gels were run in triplicate to assess the method of preparation yielding the least variability. Number of spots and variability were different between conditions. Proteins solubilized in a buffer containing 5 M urea, 2 M thiourea, 2% CHAPS, 2% SB 3-10, ampholytes, DTT, and protease inhibitors and focused in a buffer containing 9 M urea and 4% NP40 had the lowest coefficient of variation. Variability was compared across isoelectric point ranges and was different. Minimizing technical variability in two-dimensional polyacrylamide gel electrophoresis is critical to identify differences between conditions. Sample preparation should be optimized to minimize variability as well as to maximize the number of spots seen.     

Geographic variation in adult and embryonic desiccation tolerance in a terrestrial-breeding frog

Intraspecific variation in the ability of individuals to tolerate environmental perturbations is often neglected when considering the impacts of climate change. Yet this information is potentially crucial for mitigating deleterious effects of climate change on threatened species. Here we assessed patterns of intraspecific variation in desiccation tolerance in the frog Pseudophryne guentheri, a terrestrial-breeding species experiencing a drying climate. Adult frogs were collected from six populations across a rainfall gradient and their dehydration and rehydration rates were assessed. We also compared desiccation tolerance of embryos and hatchlings originating from within-population parental crosses from four of the populations. Embryos were reared on soil at three soil–water potentials and their desiccation tolerance was assessed across a range of traits. We found significant and strong patterns of intraspecific variation in almost all traits, both in adults and first-generation offspring. Adult frogs exhibited clinal variation in their water balance responses, with populations from drier sites both dehydrating and rehydrating more slowly compared to frogs from more mesic sites. Similarly, desiccation tolerance of first-generation offspring was significantly greater in populations from xeric sites. Our findings suggest that populations within this species will respond differently to the regional reduction in rainfall predicted by climate change models.     

Adaptation to simultaneous warming and acidification carries a thermal tolerance cost in a marine copepod

The ocean is undergoing warming and acidification. Thermal tolerance is affected both by evolutionary adaptation and developmental plasticity. Yet, thermal tolerance in animals adapted to simultaneous warming and acidification is unknown. We experimentally evolved the ubiquitous copepod Acartia tonsa to future combined ocean warming and acidification conditions (OWA approx. 22°C, 2000 µatm CO₂) and then compared its thermal tolerance relative to ambient conditions (AM approx. 18°C, 400 µatm CO₂). The OWA and AM treatments were reciprocally transplanted after 65 generations to assess effects of developmental conditions on thermal tolerance and potential costs of adaptation. Treatments transplanted from OWA to AM conditions were assessed at the F1 and F9 generations following transplant. Adaptation to warming and acidification, paradoxically, reduces both thermal tolerance and phenotypic plasticity. These costs of adaptation to combined warming and acidification may limit future population resilience.     

Change and stasis in marine hybrid zones in response to climate warming

Aim We test the prediction that hybrid zones between warm‐ and cold‐adapted species will move towards the territory formerly occupied by the cold‐adapted species in response to a warming climate. We use multiple tests of this prediction to distinguish amongst potential mechanistic hypotheses of responses to climate change. Location We sampled 97 locations on the Atlantic coast of Spain and France and the English Channel that span three hybrid zones formed between two species of marine mussels (Mytilus galloprovincialis and M. edulis). Methods Mussels were sampled in 2005–07 and analysed at a nuclear gene (Glu‐5′) that is diagnostically differentiated between the subject species. Results were compared to those of studies made in the same region over the past two decades. Historical change in sea surface temperature (SST) was analysed using National Oceanic and Atmospheric Administration (NOAA) Optimum Interpolation Daily SST. Species distribution models (random forest and maximum entropy) of the current distribution of mussels were constructed and validated by hindcasting the historical distributions of these species. Validated models were used in combination with forecasts of SST to predict changes in mussel distribution to 2050 and 2100. Results We show that over the past two decades two of the hybrid zones in France have not changed in either position or shape. The third hybrid zone, however, has shifted in the predicted direction, c. 100 km eastward into the warming English Channel. Species distribution modelling strongly implicates changes in winter cold SST as driving this change in the position of one of the hybrid zones. Forecasts of future SST indicate that rapid changes in distribution will occur over the next century. Main conclusions Hybrid zones can be used to conduct repeated tests of ecological responses to climate change and can be valuable in sorting among prospective mechanistic hypotheses that underlie that change. Winter temperatures, but not seasonal high temperature, appear to control the distribution of both species. Species distribution modelling indicates that the collapse of these hybrid zones is imminent, with the rapid expansion of the subtropical species in response to continuing SST warming.     

Unshelled abalone and corrupted urchins: development of marine calcifiers in a changing ocean

The most fragile skeletons produced by benthic marine calcifiers are those that larvae and juveniles make to support their bodies. Ocean warming, acidification, decreased carbonate saturation and their interactive effects are likely to impair skeletogenesis. Failure to produce skeleton in a changing ocean has negative implications for a diversity of marine species. We examined the interactive effects of warming and acidification on an abalone (Haliotis coccoradiata) and a sea urchin (Heliocidaris erythrogramma) reared from fertilization in temperature and pH/pCO(2) treatments in a climatically and regionally relevant setting. Exposure of ectodermal (abalone) and mesodermal (echinoid) calcifying systems to warming (+2°C to 4°C) and acidification (pH 7.6-7.8) resulted in unshelled larvae and abnormal juveniles. Haliotis development was most sensitive with no interaction between stressors. For Heliocidaris, the percentage of normal juveniles decreased in response to both stressors, although a +2°C warming diminished the negative effect of low pH. The number of spines produced decreased with increasing acidification/pCO(2), and the interactive effect between stressors indicated that a +2°C warming reduced the negative effects of low pH. At +4°C, the developmental thermal tolerance was breached. Our results show that projected near-future climate change will have deleterious effects on development with differences in vulnerability in the two species.     

Stress tolerance in a novel system: Genetic and environmental sources of (co)variation for cold tolerance in the butterfly Eurema smilax

The physiological ability to survive climatic extremes, such as low temperature, is a major determinant of species distribution. Research suggests that tropically restricted insect populations may possess low to zero variation in stress tolerance, thereby limiting any potential to adapt to colder climates. This paradigm derives largely from contrasts among Drosophila populations and species along the tropical–temperate cline of eastern Australia. Butterfly groups, such as the variously distributed representatives of the genus Eurema, offer opportunities to test the taxonomic breadth of this paradigm. We contribute here by investigating plasticity, repeatability and heritability (h²) for cold tolerance in Eurema smilax. This continentally widespread species (extending from the Torres Strait to the south coast of Victoria) offers an important comparative basis for evaluating stress tolerance in geographically restricted congenerics. We reared two generations of E. smilax under laboratory conditions and measured recovery from a chill‐coma assay, which is one of the commonly used methods for characterizing adult cold stress tolerance. Trials on F2s conducted over three consecutive days revealed individual repeatability (r = 0.405). However, recovery time decreased systematically across trials, which is characteristic of a phenotypically plastic ‘hardening’ response to prior cold exposure. Generalized linear modelling, wherein genetic variance was estimated via an ‘animal model’ approach, indicated no difference between sexes and no effect of body size, but a significant additive genetic term, corresponding to a heritability estimate of h² = 0.414 ± 0.100. These data suggest significant adaptive potential for cold tolerance in E. smilax but show that individuals may also respond directly to extremes of cold via phenotypic plasticity. This indicates the potential to adapt to varied thermal extremes, which would be expected for a broadly distributed species that is resilient to climate change.     

Hypoxia tolerance associated with activity reduction is a key adaptation for Laternula elliptica seasonal energetics

Seasonal dormancy is a widespread mechanism for reducing energy expenditure during periods of low energy availability. Seasonal variation in activity and the cost of pumping water through the siphons were investigated to estimate the importance of activity regulation to the seasonal energy budget of the Antarctic clam, Laternula elliptica. In the laboratory, a metabolic rate of 26.35 μmol O₂ h⁻¹ was estimated for a 50-mm shell length L. elliptica pumping water at −0.4 °C. In the field, the proportion of time siphons were visible at the sediment surface varied seasonally (32% visible in June/July compared to 86% in December/January). L. elliptica were actively pumping for a minimum of 19% of each 24-h period during winter (August) compared to a summer maximum when animals were actively pumping for 73% of the time (February). This resulted in a 3.7-fold seasonal difference in the calculated energy consumption of a 50-mm L. elliptica (19.2 μmol O₂ h⁻¹ in February versus 5.0 μmol O₂ h⁻¹ in August), which closely matches the 3.0-fold seasonal variation in metabolic rate found previously. Seasonal variation in activity could therefore be responsible for much of the seasonal difference in energy consumption of L. elliptica. Inter-annual variation in timing of the seasonal activity maxima (January 2004 and March 1999) was correlated with variation in the timing of the summer plankton bloom in Ryder Bay. In the laboratory, periods of extended siphon closure (133 ± 114 min, mean ± SD) were accompanied by long periods of heart arrhythmia (167 ± 135 min), during which time blood oxygen levels dropped to values close to zero. Heart arrhythmia is most likely part of a hypo-metabolic adaptation to reduce energy costs during extended periods of siphon closure. Physiological and behavioural dormancy, with associated hypoxia tolerance, appear to be key mechanisms controlling the seasonal energy budget of L. elliptica.     

Bet hedging in a warming ocean: predictability of maternal environment shapes offspring size variation in marine sticklebacks

Bet hedging at reproduction is expected to evolve when mothers are exposed to unpredictable cues for future environmental conditions, whereas transgenerational plasticity (TGP) should be favoured when cues reliably predict the environment offspring will experience. Since climate predictions forecast an increase in both temperature and climate variability, both TGP and bet hedging are likely to become important strategies to mediate climate change effects. Here, the potential to produce variably sized offspring in both warming and unpredictable environments was tested by investigating whether stickleback (Gasterosteus aculeatus) mothers adjusted mean offspring size and within‐clutch variation in offspring size in response to experimental manipulation of maternal thermal environment and predictability (alternating between ambient and elevated water temperatures). Reproductive output traits of F1 females were influenced by both temperature and environmental predictability. Mothers that developed at ambient temperature (17 °C) produced larger, but fewer eggs than mothers that developed at elevated temperature (21 °C), implying selection for different‐sized offspring in different environments. Mothers in unpredictable environments had smaller mean egg sizes and tended to have greater within‐female egg size variability, especially at 21 °C, suggesting that mothers may have dynamically modified the variance in offspring size to spread the risk of incorrectly predicting future environmental conditions. Both TGP and diversification influenced F2 offspring body size. F2 offspring reared at 21 °C had larger mean body sizes if their mother developed at 21 °C, but this TGP benefit was not present for offspring of 17 °C mothers reared at 17 °C, indicating that maternal TGP will be highly relevant for ocean warming scenarios in this system. Offspring of variable environment mothers were smaller but more variable in size than offspring from constant environment mothers, particularly at 21 °C. In summary, stickleback mothers may have used both TGP and diversified bet‐hedging strategies to cope with the dual stress of ocean warming and environmental uncertainty.     

Recent changes in the distribution of a marine gastropod,Patella rustica Linnaeus, 1758, and their relationship to unusual climatic events

Aim Recent colonization of northern Portuguese shores by Patella rustica Linnaeus, 1758, led to the bridging of a historical gap in the distribution known since the 1900s. Long‐term oceanographic data collected over the last half‐century were examined in order to detect possible mechanisms for the observed change in its distribution. Location This study was carried out along the entire Portuguese coastline, from 41°50′ to 37°06′ N. Time‐series of hydrographical variables (sea surface temperature and salinity) were derived for the Atlantic coast of the Iberian Peninsula. Methods Abundance and size‐frequency distributions of the newly observed limpet populations were compared with those from well‐established populations in southern Portugal. Anomalies were computed for sea surface temperature (1950–2000) and sea surface salinity (1958–2001) data, covering the whole Atlantic coast of the Iberian Peninsula. An upwelling index (1967–2005) was derived for a single location within the distributional gap of P. rustica. Split moving window analysis was performed to detect significant discontinuities in hydrographical data sets. Results Patella rustica has gradually been expanding in northern Iberia, and in the late 1990s the historical gap in distribution in northern Portugal was bridged. Size‐frequency distribution differed between historical and recent populations, the latter lacking small‐sized individuals. At the same time, several anomalous oceanographic events occurred off the Portuguese coast and were probably related to this expansion. Main conclusions Although sea surface temperature might be a major determinant of the reproductive success of P. rustica and hence its dispersal potential, it is more likely that a coincidence of several factors occurring in the late 1990s provided exceptional conditions that allowed the geographical expansion of this species.     

Heritable variation in heat shock gene expression: a potential mechanism for adaptation to thermal stress in embryos of sea turtles

The capacity of species to respond adaptively to warming temperatures will be key to their survival in the Anthropocene. The embryos of egg-laying species such as sea turtles have limited behavioural means for avoiding high nest temperatures, and responses at the physiological level may be critical to coping with predicted global temperature increases. Using the loggerhead sea turtle (Caretta caretta) as a model, we used quantitative PCR to characterise variation in the expression response of heat-shock genes (hsp60, hsp70 and hsp90; molecular chaperones involved in cellular stress response) to an acute non-lethal heat shock. We show significant variation in gene expression at the clutch and population levels for some, but not all hsp genes. Using pedigree information, we estimated heritabilities of the expression response of hsp genes to heat shock and demonstrated both maternal and additive genetic effects. This is the first evidence that the heat-shock response is heritable in sea turtles and operates at the embryonic stage in any reptile. The presence of heritable variation in the expression of key thermotolerance genes is necessary for sea turtles to adapt at a molecular level to warming incubation environments.     

Parasitism in early life: environmental conditions shape within‐brood variation in responses to infection

Parasites play key ecological and evolutionary roles through the costs they impose on their host. In wild populations, the effect of parasitism is likely to vary considerably with environmental conditions, which may affect the availability of resources to hosts for defense. However, the interaction between parasitism and prevailing conditions is rarely quantified. In addition to environmental variation acting on hosts, individuals are likely to vary in their response to parasitism, and the combined effect of both may increase heterogeneity in host responses. Offspring hierarchies, established by parents in response to uncertain rearing conditions, may be an important source of variation between individuals. Here, we use experimental antiparasite treatment across 5 years of variable conditions to test how annual population productivity (a proxy for environmental conditions) and parasitism interact to affect growth and survival of different brood members in juvenile European shags (Phalacrocorax aristotelis). In control broods, last‐hatched chicks had more plastic growth rates, growing faster in more productive years. Older siblings grew at a similar rate in all years. Treatment removed the effect of environment on last‐hatched chicks, such that all siblings in treated broods grew at a similar rate across environmental conditions. There were no differences in nematode burden between years or siblings, suggesting that variation in responses arose from intrinsic differences between chicks. Whole‐brood growth rate was not affected by treatment, indicating that within‐brood differences were driven by a change in resource allocation between siblings rather than a change in overall parental provisioning. We show that gastrointestinal parasites can be a key component of offspring's developmental environment. Our results also demonstrate the value of considering prevailing conditions for our understanding of parasite effects on host life‐history traits. Establishing how environmental conditions shape responses to parasitism is important as environmental variability is predicted to increase.     

Genetic selection on a behavioural fear trait is associated with changes in heart rate variability in quail

This study investigated whether genetic selection on a divergent behavioural trait of fearfulness (tonic immobility duration) was related to changes in the nervous control of the heart. Quail selected for either long or short tonic immobility (LTI or STI, respectively) duration was compared with an unselected control line (CTI). The autonomic control of the heart was assessed by heart rate variability analysis and pharmacological blockades. Quail were surgically fitted with a telemetric device. Heart rate before injection did not differ between the three lines. The vagal-sympathetic effect (VSE) at rest differed significantly from 1 in CTI and STI quail, suggesting that parasympathetic activity was dominant. In LTI quail, VSE did not differ from 1, suggesting a balance between parasympathetic and sympathetic activities. The intrinsic heart rate reached after the successive injections of propranolol and atropine did not differ between lines and was higher than the heart rate at rest in STI, which was in line with results of VSE at rest. After atropine injection, the sympathetic activity indicated by the low-frequency power was lower in CTI than in the two selected quail. After propranolol injection, the parasympathetic activity indicated by the root of the mean squares of successive differences and the high-frequency power was higher in STI than in CTI and LTI quail. Selection on tonic immobility duration thus appears to be associated with changes in the sympathovagal control of the heart, which may influence behavioural responses to stressful situations.     

Late‐season snowfall is associated with decreased offspring survival in two migratory arctic‐breeding songbird species

While the effect of weather on reproduction has been studied for many years in avian taxa, the rapid pace of climate change in arctic regions has added urgency to this question by changing the weather conditions species experience during breeding. Given this, it is important to understand how factors such as temperature, rain, snowfall, and wind affect reproduction both directly and indirectly (e.g. through their effects on food availability). In this study, we ask how weather factors and food availability influence daily survival rates of clutches in two arctic‐breeding migratory songbirds: the Lapland longspur Calcarius lapponicus, a circumpolar breeder, and Gambel's white‐crowned sparrow Zonotrichia leucophrys gambelii, which breeds in shrubby habitats across tundra, boreal and continental climates. To do this, we monitored clutch survival in these two species from egg‐lay through fledge at field sites located near Toolik Field Station (North Slope, Alaska) across 5 yr (2012–2016). Our results indicate that snowfall and cold temperatures decreased offspring survival rates in both species; although Lapland longspurs were more susceptible to snowfall. Food availability, quantified by pitfall sampling and sweep‐net sampling methods, had minimal effects on offspring survival. Some climate models predict increased precipitation for the Arctic with global warming, and in the Toolik region, total snow accumulation may be increasing. Placed in this context, our results suggest that changes in snow storms with climate change could have substantial consequences for reproduction in migratory songbirds breeding in the North American Arctic.     

Integrating patterns of thermal tolerance and phenotypic plasticity with population genetics to improve understanding of vulnerability to warming in a widespread copepod

Differences in population vulnerability to warming are defined by spatial patterns in thermal adaptation. These patterns may be driven by natural selection over spatial environmental gradients, but can also be shaped by gene flow, especially in marine taxa with high dispersal potential. Understanding and predicting organismal responses to warming requires disentangling the opposing effects of selection and gene flow. We begin by documenting genetic divergence of thermal tolerance and developmental phenotypic plasticity. Ten populations of the widespread copepod Acartia tonsa were collected from sites across a large thermal gradient, ranging from the Florida Keys to Northern New Brunswick, Canada (spanning over 20° latitude). Thermal performance curves (TPCs) from common garden experiments revealed local adaptation at the sampling range extremes, with thermal tolerance increasing at low latitudes and decreasing at high latitudes. The opposite pattern was observed in phenotypic plasticity, which was strongest at high latitudes. No relationship was observed between phenotypic plasticity and environmental variables. Instead, the results are consistent with the hypothesis of a trade‐off between thermal tolerance and the strength of phenotypic plasticity. Over a large portion of the sampled range, however, we observed a remarkable lack of differentiation of TPCs. To examine whether this lack of divergence is the result of selection for a generalist performance curve or constraint by gene flow, we analyzed cytochrome oxidase I mtDNA sequences, which revealed four distinct genetic clades, abundant genetic diversity, and widely distributed haplotypes. Strong divergence in thermal performance within genetic clades, however, suggests that the pace of thermal adaptation can be relatively rapid. The combined insight from the laboratory physiological experiments and genetic data indicate that gene flow constrains differentiation of TPCs. This balance between gene flow and selection has implications for patterns of vulnerability to warming. Taking both genetic differentiation and phenotypic plasticity into account, our results suggest that local adaptation does not increase vulnerability to warming, and that low‐latitude populations in general may be more vulnerable to predicted temperature change over the next century.     

Bill size variation in northern cardinals associated with anthropogenic drivers across North America

Allen's rule predicts that homeotherms inhabiting cooler climates will have smaller appendages, while those inhabiting warmer climates will have larger appendages relative to body size. Birds’ bills tend to be larger at lower latitudes, but few studies have tested whether modern climate change and urbanization affect bill size. Our study explored whether bill size in a wide‐ranging bird would be larger in warmer, drier regions and increase with rising temperatures. Furthermore, we predicted that bill size would be larger in densely populated areas, due to urban heat island effects and the higher concentration of supplementary foods. Using measurements from 605 museum specimens, we explored the effects of climate and housing density on northern cardinal bill size over an 85‐year period across the Linnaean subspecies’ range. We quantified the geographic relationships between bill surface area, housing density, and minimum temperature using linear mixed effect models and geographically weighted regression. We then tested whether bill surface area changed due to housing density and temperature in three subregions (Chicago, IL., Washington, D.C., and Ithaca, NY). Across North America, cardinals occupying drier regions had larger bills, a pattern strongest in males. This relationship was mediated by temperature such that birds in warm, dry areas had larger bills than those in cool, dry areas. Over time, female cardinals’ bill size increased with warming temperatures in Washington, D.C., and Ithaca. Bill size was smaller in developed areas of Chicago, but larger in Washington, D.C., while there was no pattern in Ithaca, NY. We found that climate and urbanization were strongly associated with bill size for a wide‐ranging bird. These biogeographic relationships were characterized by sex‐specific differences, varying relationships with housing density, and geographic variability. It is likely that anthropogenic pressures will continue to influence species, potentially promoting microevolutionary changes over space and time.