Abstract
Global temperature changes have emphasized the need to understand how species adapt to thermal stress across their ranges. Genetic mechanisms may contribute to variation in thermal tolerance, providing evidence for how organisms adapt to local environments. We determine physiological thermal limits and characterize genome-wide transcriptional changes at these limits in bumble bees using laboratory-reared Bombus vosnesenskii workers. We analyze bees reared from latitudinal (35.7–45.7°N) and altitudinal (7–2154 m) extremes of the species’ range to correlate thermal tolerance and gene expression among populations from different climates. We find that critical thermal minima (CTMIN) exhibit strong associations with local minimums at the location of queen origin, while critical thermal maximum (CTMAX) was invariant among populations. Concordant patterns are apparent in gene expression data, with regional differentiation following cold exposure, and expression shifts invariant among populations under high temperatures. Furthermore, we identify several modules of co-expressed genes that tightly correlate with critical thermal limits and temperature at the region of origin. Our results reveal that local adaptation in thermal limits and gene expression may facilitate cold tolerance across a species range, whereas high temperature responses are likely constrained, both of which may have implications for climate change responses of bumble bees.
Highlights
Global temperature changes have emphasized the need to understand how species adapt to thermal stress across their ranges
Laboratory colonies of Bombus vosnesenskii were established from wild queens collected from four regions: low-elevation CA (L-CA), high-elevation CA (H-CA), low-elevation OR (L-OR), and high-elevation OR (H-OR) (Fig. 1A, “SI Appendix”, Table S1), with each region representing a distinct thermal environment, as highlighted by mean monthly temperature over the course of an average year (Fig. 1B). CTMIN of laboratory-reared B. vosnesenskii workers varied significantly with region of origin (ANOVA, F 3,8 = 8.6, P = 0.007; Table S2; Dataset S1), with bees from colder regions having reduced CTMIN (Fig. 1C)
We performed RNAseq on bees from the CTMIN and CTMAX experiments plus untreated controls, and first explored the data by determining best fit general linear models for expression patterns for samples grouped by geographic region (L-CA, H-CA, L-OR, H-OR) or treatment (CTMIN, CTMAX, control) with the Akaike Information Criterion (AIC)[41]
Summary
Global temperature changes have emphasized the need to understand how species adapt to thermal stress across their ranges. Our results reveal that local adaptation in thermal limits and gene expression may facilitate cold tolerance across a species range, whereas high temperature responses are likely constrained, both of which may have implications for climate change responses of bumble bees. Studies have revealed that many terrestrial ectotherms show little variation in C TMAX but pronounced differences in CTMIN with geographic temperature gradients[14,15,16] The mechanisms underlying this spatial variation in thermal limits will inform species responses to changing temperatures but have rarely been studied (but s ee[17]). Shifts in gene expression likely contribute to physiological responses that underly rangewide variation in thermal tolerances, responses that may be shaped by natural selection and limit species distributions[5,10,18]. As responses to thermal extremes may vary among populations for widely distributed species[18,32], such population variation in thermal tolerance could profoundly alter predictions of the impacts of changing climates on bumble bees
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