Maladaptive plasticity facilitates evolution of thermal tolerance during an experimental range shift
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...
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| Format: | Article |
| Language: | English |
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BMC
2020-04-01
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| Series: | BMC Evolutionary Biology |
| Subjects: | |
| Online Access: | http://link.springer.com/article/10.1186/s12862-020-1589-7 |
| _version_ | 1819007735660806144 |
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| author | Aoife M. Leonard Lesley T. Lancaster |
| author_facet | Aoife M. Leonard Lesley T. Lancaster |
| author_sort | Aoife M. Leonard |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-12-21T00:29:18Z |
| format | Article |
| id | doaj.art-82f7f3ace574442890f98cb452a7408d |
| institution | Directory Open Access Journal |
| issn | 1471-2148 |
| language | English |
| last_indexed | 2024-12-21T00:29:18Z |
| publishDate | 2020-04-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Evolutionary Biology |
| spelling | doaj.art-82f7f3ace574442890f98cb452a7408d2022-12-21T19:21:54ZengBMCBMC Evolutionary Biology1471-21482020-04-0120111110.1186/s12862-020-1589-7Maladaptive plasticity facilitates evolution of thermal tolerance during an experimental range shiftAoife M. Leonard0Lesley T. Lancaster1School of Biological Sciences, Zoology Building, University of AberdeenSchool of Biological Sciences, Zoology Building, University of AberdeenAbstract 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.http://link.springer.com/article/10.1186/s12862-020-1589-7Countergradient variationMaladaptive plasticityThermal fluctuationsRange-shiftsGenetic compensationCallosobruchus maculatus |
| spellingShingle | Aoife M. Leonard Lesley T. Lancaster Maladaptive plasticity facilitates evolution of thermal tolerance during an experimental range shift BMC Evolutionary Biology Countergradient variation Maladaptive plasticity Thermal fluctuations Range-shifts Genetic compensation Callosobruchus maculatus |
| title | Maladaptive plasticity facilitates evolution of thermal tolerance during an experimental range shift |
| title_full | Maladaptive plasticity facilitates evolution of thermal tolerance during an experimental range shift |
| title_fullStr | Maladaptive plasticity facilitates evolution of thermal tolerance during an experimental range shift |
| title_full_unstemmed | Maladaptive plasticity facilitates evolution of thermal tolerance during an experimental range shift |
| title_short | Maladaptive plasticity facilitates evolution of thermal tolerance during an experimental range shift |
| title_sort | maladaptive plasticity facilitates evolution of thermal tolerance during an experimental range shift |
| topic | Countergradient variation Maladaptive plasticity Thermal fluctuations Range-shifts Genetic compensation Callosobruchus maculatus |
| url | http://link.springer.com/article/10.1186/s12862-020-1589-7 |
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