scholarly journals Evolution, not transgenerational plasticity, explains the divergence of acorn ant thermal tolerance across an urban-rural temperature cline

2019 ◽  
Author(s):  
Ryan A. Martin ◽  
Lacy D. Chick ◽  
Aaron R. Yilmaz ◽  
Sarah E. Diamond

AbstractDisentangling the mechanisms of phenotypic shifts in response to environmental change is critical, and although studies increasingly disentangle phenotypic plasticity from evolutionary change, few explore the potential role for transgenerational plasticity in this context. Here, we evaluate the potential role that transgenerational plasticity plays in phenotypic divergence of acorn ants in response to urbanization. F2 generation worker ants (offspring of lab-born queens) exhibited similar divergence among urban and rural populations as F1 generation worker ants (offspring of field-born queens) indicating that evolutionary differentiation rather than transgenerational plasticity was responsible for shifts towards higher heat tolerance and diminished cold tolerance in urban acorn ants. Hybrid matings between urban and rural populations provided further insight into the genetic architecture of thermal adaptation. Heat tolerance of hybrids more resembled the urban-urban pure type, whereas cold tolerance of hybrids more resembled the rural-rural pure type. As a consequence, thermal tolerance traits in this system appear to be influenced by dominance rather than being purely additive traits, and heat and cold tolerance might be determined by separate genes. Though transgenerational plasticity does not explain divergence of acorn ant thermal tolerance, its role in divergence of other traits and across other urbanization gradients merits further study.

2018 ◽  
Vol 285 (1882) ◽  
pp. 20180036 ◽  
Author(s):  
Sarah E. Diamond ◽  
Lacy D. Chick ◽  
Abe Perez ◽  
Stephanie A. Strickler ◽  
Ryan A. Martin

The question of parallel evolution—what causes it, and how common it is—has long captured the interest of evolutionary biologists. Widespread urban development over the last century has driven rapid evolutionary responses on contemporary time scales, presenting a unique opportunity to test the predictability and parallelism of evolutionary change. Here we examine urban evolution in an acorn-dwelling ant species, focusing on the urban heat island signal and the ant's tolerance of these altered urban temperature regimes. Using a common-garden experimental design with acorn ant colonies collected from urban and rural populations in three cities and reared under five temperature treatments in the laboratory, we assessed plastic and evolutionary shifts in the heat and cold tolerance of F1 offspring worker ants. In two of three cities, we found evolved losses of cold tolerance, and compression of thermal tolerance breadth. Results for heat tolerance were more complex: in one city, we found evidence of simple evolved shifts in heat tolerance in urban populations, though in another, the difference in urban and rural population heat tolerance depended on laboratory rearing temperature, and only became weakly apparent at the warmest rearing temperatures. The shifts in tolerance appeared to be adaptive, as our analysis of the fitness consequences of warming revealed that while urban populations produced more sexual reproductives under warmer laboratory rearing temperatures, rural populations produced fewer. Patterns of natural selection on thermal tolerances supported our findings of fitness trade-offs and local adaptation across urban and rural acorn ant populations, as selection on thermal tolerance acted in opposite directions between the warmest and coldest rearing temperatures. Our study provides mixed support for parallel evolution of thermal tolerance under urban temperature rise, and, importantly, suggests the promising use of cities to examine parallel and non-parallel evolution on contemporary time scales.


2019 ◽  
Vol 374 (1778) ◽  
pp. 20190036 ◽  
Author(s):  
Jennifer Sunday ◽  
Joanne M. Bennett ◽  
Piero Calosi ◽  
Susana Clusella-Trullas ◽  
Sarah Gravel ◽  
...  

Linking variation in species' traits to large-scale environmental gradients can lend insight into the evolutionary processes that have shaped functional diversity and future responses to environmental change. Here, we ask how heat and cold tolerance vary as a function of latitude, elevation and climate extremes, using an extensive global dataset of ectotherm and endotherm thermal tolerance limits, while accounting for methodological variation in acclimation temperature, ramping rate and duration of exposure among studies. We show that previously reported relationships between thermal limits and latitude in ectotherms are robust to variation in methods. Heat tolerance of terrestrial ectotherms declined marginally towards higher latitudes and did not vary with elevation, whereas heat tolerance of freshwater and marine ectotherms declined more steeply with latitude. By contrast, cold tolerance limits declined steeply with latitude in marine, intertidal, freshwater and terrestrial ectotherms, and towards higher elevations on land. In all realms, both upper and lower thermal tolerance limits increased with extreme daily temperature, suggesting that different experienced climate extremes across realms explain the patterns, as predicted under the Climate Extremes Hypothesis . Statistically accounting for methodological variation in acclimation temperature, ramping rate and exposure duration improved model fits, and increased slopes with extreme ambient temperature. Our results suggest that fundamentally different patterns of thermal limits found among the earth's realms may be largely explained by differences in episodic thermal extremes among realms, updating global macrophysiological ‘rules’. This article is part of the theme issue ‘Physiological diversity, biodiversity patterns and global climate change: testing key hypotheses involving temperature and oxygen’.


2017 ◽  
Author(s):  
Brent L. Lockwood ◽  
Tarun Gupta ◽  
Rosemary Scavotto

AbstractMany terrestrial ectothermic species exhibit limited variation in upper thermal tolerance across latitude. However, these trends may not signify limited adaptive capacity to increase thermal tolerance in the face of climate change. Instead, thermal tolerance may be similar among populations because behavioral thermoregulation by mobile organisms or life stages may buffer natural selection for thermal tolerance. We compared thermal tolerance of adults and embryos among natural populations of Drosophila melanogaster from a broad range of thermal habitats around the globe to assess natural variation of thermal tolerance in mobile vs. immobile life stages. We found no variation among populations in adult thermal tolerance, but embryonic thermal tolerance was higher in tropical strains than in temperate strains. Average maximum temperature of the warmest month of the year predicted embryonic thermal tolerance in tropical but not temperate sites. We further report that embryos live closer to their upper thermal limits than adultso—i.e., thermal safety margins are smaller for embryos than adults. F1 hybrid embryos from crosses between temperate and tropical populations had thermal tolerance that matched that of tropical embryos, suggesting dominance of heat-tolerant alleles. Together our findings suggest that thermal selection has led to divergence in embryonic thermal tolerance but that selection for divergent thermal tolerance may be limited in adults. Further, our results suggest that thermal traits should be measured across life stages in order to better predict adaptive limits.Impact SummaryClimate change may threaten the extinction of many ectothermic species, unless populations can evolutionarily adapt to rising temperatures. Natural selection should favor individuals with higher heat tolerances in hotter environments. But recent studies have found that individuals from hot and cold places often have similar heat tolerances. This pattern may indicate that the evolution of heat tolerance is constrained. If this were true, then it would have dire consequences for species persistence under novel thermal conditions.An alternative explanation for lack of variation in heat tolerance is that mobile organisms don’t need higher heat tolerances to survive in hotter places. The majority of studies have focused on heat tolerance of the adult life stage. Yet, adults in many species are mobile organisms that can avoid extreme heat by seeking shelter in cooler microhabitats (e.g., shaded locations). In contrast, immobile life stages (e.g., insect eggs) cannot behaviorally avoid extreme heat. Thus, mobile and immobile life stages may face different thermal selection pressures that lead to disparate patterns of thermal adaptation across life stages.Here, we compared heat tolerances of fruit fly adults and eggs (Drosophila melanogaster) from populations in temperate North America and tropical locations around the globe. Consistent with previous studies, we found no differences among populations in adult heat tolerance. However, eggs from tropical flies were consistently more heat tolerant than eggs from North American flies. Further, eggs had lower heat tolerance than adults. Consequently, fly eggs in the hotter tropics may experience heat death more frequently than adult flies later in life. This may explain why patterns of divergence in heat tolerance were decoupled across life stages. These patterns indicate that thermal adaptation may be life-stage-specific and suggest that future work should characterize thermal traits across life stages to better understand the evolution of thermal limits.


2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Joanne M. Bennett ◽  
Jennifer Sunday ◽  
Piero Calosi ◽  
Fabricio Villalobos ◽  
Brezo Martínez ◽  
...  

AbstractUnderstanding how species’ thermal limits have evolved across the tree of life is central to predicting species’ responses to climate change. Here, using experimentally-derived estimates of thermal tolerance limits for over 2000 terrestrial and aquatic species, we show that most of the variation in thermal tolerance can be attributed to a combination of adaptation to current climatic extremes, and the existence of evolutionary ‘attractors’ that reflect either boundaries or optima in thermal tolerance limits. Our results also reveal deep-time climate legacies in ectotherms, whereby orders that originated in cold paleoclimates have presently lower cold tolerance limits than those with warm thermal ancestry. Conversely, heat tolerance appears unrelated to climate ancestry. Cold tolerance has evolved more quickly than heat tolerance in endotherms and ectotherms. If the past tempo of evolution for upper thermal limits continues, adaptive responses in thermal limits will have limited potential to rescue the large majority of species given the unprecedented rate of contemporary climate change.


PeerJ ◽  
2019 ◽  
Vol 7 ◽  
pp. e7060 ◽  
Author(s):  
Karina Sánchez-Echeverría ◽  
Ignacio Castellanos ◽  
Luis Mendoza-Cuenca ◽  
Iriana Zuria ◽  
Gerardo Sánchez-Rojas

Urbanization is one of the most significant land cover transformations, and while climate alteration is one of its most cited ecological consequences we have very limited knowledge on its effect on species’ thermal responses. We investigated whether changes in environmental thermal variability caused by urbanization influence thermal tolerance in honey bees (Apis mellifera) in a semi-arid city in central Mexico. Ambient environmental temperature and honey bee thermal tolerance were compared in urban and rural sites. Ambient temperature variability decreased with urbanization due to significantly higher nighttime temperatures in urban compared to rural sites and not from differences in maximum daily temperatures. Honey bee thermal tolerance breadth [critical thermal maxima (CTmax)—critical thermal minima (CTmin)] was narrower for urban bees as a result of differences in cold tolerance, with urban individuals having significantly higher CTminthan rural individuals, and CTmaxnot differing among urban and rural individuals. Honey bee body size was not correlated to thermal tolerance, and body size did not differ between urban and rural individuals. We found that honey bees’ cold tolerance is modified through acclimation. Our results show that differences in thermal variability along small spatial scales such as urban-rural gradients can influence species’ thermal tolerance breadths.


PeerJ ◽  
2017 ◽  
Vol 5 ◽  
pp. e3112 ◽  
Author(s):  
Thomas Enriquez ◽  
Hervé Colinet

The spotted wing Drosophila,Drosophila suzukii, is a new pest in Europe and America which causes severe damages, mostly to stone fruit crops. Temperature and humidity are among the most important abiotic factors governing insect development and fitness. In many situations, temperature can become stressful thus compromising survival. The ability to cope with thermal stress depends on basal level of thermal tolerance. Basic knowledge on temperature-dependent mortality ofD. suzukiiis essential to facilitate management of this pest. The objective of the present study was to investigateD. suzukiibasal cold and heat tolerance. Adults and pupae were subjected to six low temperatures (−5–7.5 °C) and seven high temperatures (30–37 °C) for various durations, and survival-time-temperature relationships were investigated. Data showed that males were globally more cold tolerant than females. At temperature above 5 °C, adult cold mortality became minor even after prolonged exposures (e.g., only 20% mortality after one month at 7.5 °C). Heat tolerance of males was lower than that of females at the highest tested temperatures (34, 35 and 37 °C). Pupae appeared much less cold tolerant than adults at all temperatures (e.g., Lt50at 5° C: 4–5 d for adultsvs.21 h for pupae). Pupae were more heat tolerant than adults at the most extreme high temperatures (e.g., Lt50at 37 °C: 30 min for adultsvs.4 h for pupae). The pupal thermal tolerance was further investigated under lowvs.high humidity. Low relative humidity did not affect pupal cold survival, but it reduced survival under heat stress. Overall, this study shows that survival ofD. suzukiiunder heat and cold conditions can vary with stress intensity, duration, humidity, sex and stage, and the methodological approach used here, which was based on thermal tolerance landscapes, provides a comprehensive description ofD. suzukiithermal tolerance and limits.


2020 ◽  
Author(s):  
Sonya Geange ◽  
Pieter Arnold ◽  
Alexandra Catling ◽  
Onoriode Coast ◽  
Alicia Cook ◽  
...  

<p>Extreme temperature events are increasing in frequency and intensity across the globe. These extremes, rather than averages, drive species evolution and determine survival by profoundly changing the structure and fluidity of cell membranes, altering enzyme function, and denaturing proteins. Given not only our dependence on agricultural crops and natural vegetation, but also the role of photosynthetic processes within the carbon and hydrological cycles, it is imperative to assess the state of our understanding of the potential impacts of extreme events on plants. Scaling responses from the molecular and organ level to ecosystem function is not without challenge however. There is vast literature on plant thermal tolerance research, but the body of literature is so large, the approaches so disparate and often siloed among disciplines, that research in this field risks floundering at a critical time. We conducted a systematic review of more than 21,500 studies spanning over 100 years of research that yielded almost 1,700 included studies on the tolerance of cultivated and wild land plants to both heat and cold. Our review indicates that most studies on thermal tolerance focus on the cold tolerance of cultivated species (52%) and only a trivial percentage of studies have considered both heat and cold tolerance of any given species (~5%). Combined heat and cold tolerance are important in areas where plants are exposed to extremes of both or may be in the future. This review illustrates the global distribution and concentrations of thermal tolerance studies and the diversity of thermal tolerance methods, ranging from molecular to biochemical, physiological and physical examinations, from transgenic model plants to agricultural and horticultural crops, to natural forest trees, shrubs, and grassland herbs. Critically, it also demonstrates that methods and metrics for assessing thermal tolerance are far from standardised, such that our potential to achieve mechanistic insight and compare across species and biomes is compromised. Without reconciling these issues, the scope for incorporating this critical ecological information into vegetation elements of land surface models may be limited. To aid this, we identify priorities for achieving efficient, reliable, and repeatable research across the spectrum of plant thermal tolerance. These priorities, including meta-analytical approaches and comparative experimental work, will not only further fundamental plant science, but will prove essential next steps if we are to integrate such diverse data on a critical plant functional trait into a usable metric within biogeochemical models.</p>


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