Abstract
Background
Many organisms are responding to climate change with dramatic range shifts, involving plastic and genetic changes to cope with novel climate regimes found at higher latitudes. Using experimental lineages of the seed beetle Callosobruchus maculatus, we simulated the initial phase of colonisation to progressively cooler and/or more variable conditions, to investigate how adaptation and phenotypic plasticity contribute to shifts in thermal tolerance during colonisation of novel climates.
Results
We show that heat and cold tolerance rapidly evolve during the initial stages of adaptation to progressively cooler and more variable climates. The evolved shift in cold tolerance is, however, associated with maladaptive plasticity under the novel conditions, resulting in a pattern of countergradient variation between the ancestral and novel, fluctuating thermal environment. In contrast, lineages exposed to progressively cooler, but constant, temperatures over several generations expressed only beneficial plasticity in cold tolerances and no evolved response.
Conclusions
We propose that thermal adaptation during a range expansion to novel, more variable climates found at high latitudes and elevations may typically involve genetic compensation arising from maladaptive plasticity in the initial stages of adaptation, and that this form of (countergradient) thermal adaptation may represent an opportunity for more rapid and labile evolutionary change in thermal tolerances than via classic genetic assimilation models for thermal tolerance evolution (i.e., selection on existing reaction norms). Moreover, countergradient variation in thermal tolerances may typically mask cryptic genetic variability for these traits, resulting in apparent evolutionary stasis in thermal traits.
Many organisms are responding to climate change with dramatic range shifts, involving plastic and genetic changes to cope with novel climate regimes found at higher latitudes. Using experimental lineages of the seed beetle Callosobruchus maculatus, we simulated the initial phase of colonisation to progressively cooler and/or more variable conditions, to investigate how adaptation and phenotypic plasticity contribute to shifts in thermal tolerance during colonisation of novel climates.
Results
We show that heat and cold tolerance rapidly evolve during the initial stages of adaptation to progressively cooler and more variable climates. The evolved shift in cold tolerance is, however, associated with maladaptive plasticity under the novel conditions, resulting in a pattern of countergradient variation between the ancestral and novel, fluctuating thermal environment. In contrast, lineages exposed to progressively cooler, but constant, temperatures over several generations expressed only beneficial plasticity in cold tolerances and no evolved response.
Conclusions
We propose that thermal adaptation during a range expansion to novel, more variable climates found at high latitudes and elevations may typically involve genetic compensation arising from maladaptive plasticity in the initial stages of adaptation, and that this form of (countergradient) thermal adaptation may represent an opportunity for more rapid and labile evolutionary change in thermal tolerances than via classic genetic assimilation models for thermal tolerance evolution (i.e., selection on existing reaction norms). Moreover, countergradient variation in thermal tolerances may typically mask cryptic genetic variability for these traits, resulting in apparent evolutionary stasis in thermal traits.
Original language | English |
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Article number | 47 |
Number of pages | 11 |
Journal | BMC Evolutionary Biology |
Volume | 20 |
DOIs | |
Publication status | Published - 23 Apr 2020 |
Bibliographical note
Availability of data and materialsAll data generated or analysed during this study are included in this published article [and its Additional file 2].
Acknowledgements
Thank you to P. Eady for providing C. maculatus to initiate our laboratory population and advice on rearing them. Thank you to Max Schmid for commenting on an earlier version of the ms.
Funding
This research was funded by a doctoral training grant from the BBSRC-EastBio doctoral training partnership. The funding bodies played no role in the design of the study and collection, analysis, and interpretation of data and in writing the manuscript.
Keywords
- Countergradient variation
- Maladaptive plasticity
- Thermal fluctuations
- Range-shifts
- Genetic compensation
- Callosobruchus maculatus
- PHENOTYPIC PLASTICITY
- CLIMATE-CHANGE
- VARIABILITY
- HEAT
- RESPONSES
- TEMPERATURE
- ADAPTATION
- COUNTERGRADIENT VARIATION
- GENE-EXPRESSION
- STRESS