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.
Urban-driven evolution is widely evident, but whether these changes confer fitness benefits and thus represent adaptive urban evolution is less clear. We performed a multiyear field reciprocal ...transplant experiment of acorn-dwelling ants across urban and rural environments. Fitness responses were consistent with local adaptation: we found a survival advantage of the “home” and “local” treatments compared to “away” and “foreign” treatments. Seasonal bias in survival was consistent with evolutionary patterns of gains and losses in thermal tolerance traits across the urbanization gradient. Rural ants in the urban environment were more vulnerable in the summer, putatively due to low heat tolerance, and urban ants in the rural environment were more vulnerable in winter, putatively due to an evolved loss of cold tolerance. The results for fitness via fecundity were also generally consistent with local adaptation, if somewhat more complex. Urban-origin ants produced more alates in their home versus away environment, and rural-origin ants had a local advantage in the rural environment. Overall, the magnitude of local adaptation was lower for urban ants in the novel urban environment compared with rural ants adapted to the ancestral rural environment, adding further evidence that species might not keep pace with anthropogenic change.
For many species, the timing of life cycle events is advancing under contemporary global climate change. However, much less is known regarding phenological shifts as a result of other sources of ...anthropogenic change, such as urban warming. In both cases, progress has been hampered by a focus on phenological traits such as the timing of emergence, rather than the phenology of more directly related fitness traits such as the timing of reproduction. Here we explore how urban heat island effects shape the timing of reproduction in an acorn-dwelling ant. We used a common garden experiment with acorn ants collected from three cities in the eastern United States along a latitudinal gradient and reared long-term in the laboratory under five temperature treatments. This allowed us to quantify the effects of temperature on reproductive phenology across three scales—a biogeographic temperature cline, three urban vs. rural temperature comparisons, and five laboratory rearing temperatures. At our northernmost and southernmost cities (spanning 6° of latitude), we found both urbanization and warmer laboratory rearing temperature significantly advanced reproductive phenology; ants from the lowest latitude city also had earlier reproductive phenology compared with the higher latitude cities. In the field, the differences in urban versus rural acorn ant reproductive phenology translate to approximately one month earlier reproduction in the urban populations. For insects with synchronous mating events, such as ants, shifts in the already short window of time to reproduce could limit mating across environments, potentially leading to reproductive isolation between urban and rural populations.
•Warmer temperatures change the timing of life cycle events.•Urban heat island effects increase temperatures in cities compared to rural areas.•Urbanization and warmer lab rearing temperatures advanced reproductive phenology.•Reproduction advanced approximately one month for ants in urban populations.•Shifts in phenology could limit mating across urban and rural populations.
Metabolic rates of ectotherms are expected to increase with global trends of climatic warming. But the potential for rapid, compensatory evolution of lower metabolic rate in response to rising ...temperatures is only starting to be explored. Here, we explored rapid evolution of metabolic rate and locomotor performance in acorn‐dwelling ants (Temnothorax curvispinosus) in response to urban heat island effects. We reared ant colonies within a laboratory common garden (25°C) to generate a laboratory‐born cohort of workers and tested their acute plastic responses to temperature. Contrary to expectations, urban ants exhibited a higher metabolic rate compared with rural ants when tested at 25°C, suggesting a potentially maladaptive evolutionary response to urbanization. Urban and rural ants had similar metabolic rates when tested at 38°C, as a consequence of a diminished plastic response of the urban ants. Locomotor performance also evolved such that the running speed of urban ants was faster than rural ants under warmer test temperatures (32°C and 42°C) but slower under a cooler test temperature (22°C). The resulting specialist–generalist trade‐off and higher thermal optimum for locomotor performance might compensate for evolved increases in metabolic rate by allowing workers to more quickly scout and retrieve resources.
Although studies increasingly disentangle phenotypic plasticity from evolutionary responses to environmental change, few test for transgenerational plasticity in this context. Here, we evaluate ...whether phenotypic divergence of acorn ants in response to urbanization is driven by transgenerational plasticity rather than evolution. F2 generation worker ants (offspring of laboratory‐born queens) exhibited similar divergence among urban and rural populations as field‐born worker ants, suggesting that evolutionary divergence rather than transgenerational plasticity was primarily responsible for shifts toward higher heat tolerance and diminished cold tolerance in urban acorn ants. Hybrid offspring from matings between urban and rural populations also indicated that evolutionary divergence was likely the primary mechanism underlying population differences in thermal tolerance. Specifically, thermal tolerance traits were not inherited either maternally or paternally in the hybrid pairings as would be expected for strong parental or grandparental effects mediated through a single sex. Urban–rural hybrid offspring 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 appear to explain divergence of acorn ant thermal tolerance, its role in divergence of other traits and across other urbanization gradients merits further study.
Abstract
Species may exhibit similar traits via different mechanisms: environmental filtering and local adaptation (geography) and shared evolutionary history (phylogeny) can each contribute to the ...resemblance of traits among species. Parsing trait variation into geographic and phylogenetic sources is important, as each suggests different constraints on trait evolution. Here, we explore how phylogenetic distance, geographic distance, and geographic variation in climate shape physiological tolerance of high and low temperatures using a global dataset of ant thermal tolerances. We found generally strong roles for evolutionary history and geographic variation in temperature, but essentially no detectable effects of spatial proximity per se on either upper or lower thermal tolerance. When we compared the relative importance of the factors shaping upper and lower tolerances, we found a much stronger role for evolutionary history in shaping upper versus lower tolerance, and a moderately weaker role for geographic variation in temperature in shaping upper tolerance when compared with lower tolerance. Our results demonstrate how geographic variation in climate and evolutionary history may have differential effects on the upper and lower endpoints of physiological tolerance. This Janus effect, where the relative contributions of geographic variation in climate and evolutionary history are reversed for lower versus upper physiological tolerances, has gained some support in the literature, and our results for ant physiological tolerances provide further evidence of this pattern. As the climate continues to change, the high phylogenetic conservatism of upper tolerance may suggest potential constraints on the evolution of tolerance of high temperatures.
A morbidostat is a bioreactor that uses antibiotics to control the growth of bacteria, making it well-suited for studying the evolution of antibiotic resistance. However, morbidostats are often too ...expensive to be used in educational settings. Here we present a low-cost morbidostat called the EVolutionary biorEactor (EVE) that can be built by students with minimal engineering and programming experience. We describe how we validated EVE in a real classroom setting by evolving replicate Escherichia coli populations under chloramphenicol challenge, thereby enabling students to learn about bacterial growth and antibiotic resistance.
In recent years the focus in ecology has shifted from species to a greater emphasis on functional traits. In tandem with this shift, a number of trait databases have been developed covering a range ...of taxa. Here, we introduce the GlobalAnts database.
Globally, ants are dominant, diverse and provide a range of ecosystem functions. The database represents a significant tool for ecology in that it (i) contributes to a global archive of ant traits (morphology, ecology and life history) which complements existing ant databases and (ii) promotes a trait‐based approach in ant and other insect ecology through a broad set of standardised traits.
The GlobalAnts database is unique in that it represents the largest online database of functional traits with associated georeferenced assemblage‐level data (abundance and/or occupancy) for any animal group with 9056 ant species and morphospecies records for entire local assemblages across 4416 sites.
We describe the structure of the database, types of traits included and present a summary of data coverage. The value of the database is demonstrated through an initial examination of trait distributions across subfamilies, continents and biomes.
Striking biogeographic differences in ant traits are highlighted which raise intriguing questions as to the mechanisms generating them.
Because cities contain high levels of impervious surfaces and diminished buffering effects of vegetation cover, urbanized environments can warm faster over the day and exhibit more rapid warming over ...space due to greater thermal heterogeneity in these environments. Whether organismal physiologies can adapt to these more rapid spatio-temporal changes in temperature rise within cities is unknown, and exploring these responses can inform not only how plastic and evolutionary mechanisms shape organismal physiologies, but also the potential for organisms to cope with urban development. Here, we examined how plasticity in thermal tolerance under faster and slower rates of temperature change might evolve in response to the more rapid spatio-temporal temperature rise in cities. We focused on acorn ants, a temperature-sensitive, ground-dwelling ant species that makes its home inside hollowed out acorns. We reared acorn ant colonies from urban and rural populations under a common garden design in the laboratory and assessed the thermal tolerances of F1 offspring workers using both fast (1°C min
) and slow (0.2°C min
) rates of temperature change. Relative to the rural population, the urban population exhibited higher heat tolerance when the temperature was increased quickly, providing evidence that temperature ramp-rate plasticity evolved in the urban population. This result was correlated with both faster rates of diurnal warming in urban acorn ant nest sites and greater spatial heterogeneity in environmental temperature across urban foraging areas. By contrast, rates of diurnal cooling in acorn ant nest sites were similar across urban and rural habitats, and correspondingly, we found that urban and rural populations responded similarly to variation in the rate of temperature decrease when we assessed cold tolerance. Our study highlights the importance of considering not only evolutionary differentiation in trait means across urbanization gradients, but also how trait plasticity might or might not evolve.
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