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

ABSTRACT: 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.

SUBMITTER: Martin RA

PROVIDER: S-EPMC6708418 | biostudies-literature | 2019 Sep

REPOSITORIES: biostudies-literature

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

Martin Ryan A RA Chick Lacy D LD Yilmaz Aaron R AR Diamond Sarah E SE

Evolutionary applications 20190718 8

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 ...[more]

PMID: 31462922

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Project description:Atmospheric particulate matter (PM) is a recognized risk factor for the global burden of disease in human populations. We are presenting here the application of toxicogenomics in the evaluation of the toxic effects of organic content of atmospheric particle matter (PM), from urban and rural environments (city of Barcelona and village of La Pobla, NE Spain), using the developing zebrafish embryo. The main goal is to identify the metabolic pathways involved in the adverse effects observed in zebrafish embryos exposed to PM organic content from urban and rural environments, also allowing the selection of genes of interest that are differentially expressed. The relevance of particle size to the PM toxicity is also addressed. Indeed, the zebrafish embryos were exposed to PM of aerodynamic diameter larger than 7.2 Î¼m and smaller than 0.5 Î¼m (PM10 and PM0.5, respectively). PM0.5 concentrated biological and toxic activities linked to organic substances. Transcriptomic analyses showed strong induction of the AhR signalling pathway (a.k.a. dioxin-like activity) for embryos exposed to both rural and urban extracts, correlating with the concentrations of PAHs. Urban extracts, with strong contribution of traffic emissions, specifically de-regulated oxidative stress-related genes, as well as pancreatic and eye-lens specific genes, two organs known to be affected by air pollution in humans. Exposure to rural extracts, with high contribution of wood burning emissions, affected genes implicated in basic cellular functions, in agreement with their strong embryotoxicity. Extracts from rural and urban samples elicited both common and specific transcriptome responses, suggesting different potentially adverse outcomes depending on PM source and composition. The authors thank the financial support of the Spanish Ministry (project TEA-PARTICLE, grant number CGL2011-29621) and the Portuguese Foundation for Science and Technology for the doctoral grant of Sofia R. Mesquita (SFRH/BD/80710/2011) funded by the Program POPH-QREN through the Portuguese Ministry of Education and Science and the European Social Fund, and support through project PEst-C/MAR/LA0015/2013. The PM filter samples used in the present study were PM10 and PM0.5 from the urban site - total of 4 samples from 2 sampling months; and PM0.5 from the rural site - total of 2 samples from 2 sampling months (PM10 samples from the rural site were not tested due to their very low concentration in organic compounds, and insignificant biological activity, previously measured). Sampling occurred during the cold periods of the year 2012/2013. The organic fraction of PM samples was extracted by sonication using a mixture of dichloromethane:methanol. Then, the extracts were filtered, evaporated and re-dissolved in Dimethyl sulfoxide (DMSO). Zebrafish fertilized eggs were exposed to PM organic extracts (0.2% DMSO) from the urban and rural sites from 24 to 120h post-fertilization. Total RNA was isolated from whole embryos (pools of 20 individuals), using Trizol reagent protocol (Invitrogen Life Technologies, Carlsberg, CA). The microarray study was performed using the Agilent Two-colour D. rerio Oligo Microarray v3 platform, following the Agilent Microarray â?? Based Gene Expression Analysis protocol. Three biological replicates were performed for each PM sample and controls. Biological replicates, a technical replicate and a self-to-self, were simultaneously amplified and labelled using Cyanine 3 (Cy3) and Cyanine 5 (Cy5) dye. After cRNA purification (RNeasy Kit, Quiagen GmbH, Hilden, Germany), the cRNA concentration and labelling were quantified in the NanoDrop spectrophotometer, obtaining incorporation rates in the range of 15-20pmol of cyanide dye/Âµl cRNA and yield values > 0.825ug, as recommended. cRNA was fragmented and hybridized in 4x44K arrays, for 17h at 65oC. After the hybridization the array slides were washed, and immediately scanned using Microarray Scanner Agilent G2505C system. Data was extracted using Agilent Feature Extraction Software v10.5.1.1, and the quality of microarray data was evaluated using the Quality Control report provided by Agilent Software. Based on the microarray data analysis, 22 primers were selected and designed using Primer Express 2.0 software (Applied Biosystems, Foster City, CA). Genes were quantified by real-time PCR to validate the microarray data, and a subset of 13 genes were further selected by their robust behaviour in the validation assays, allowing to differentiate the toxic potential of PM from urban and rural sources.

Project description: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-1) and slow (0.2°C min-1) 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.

Dataset Information

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

Publications

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

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