Phenotypic plasticity is aligned with phenological adaptation on micro- and macroevolutionary timescales

Phenology is a key determinant of fitness, particularly in organisms with complex life cycles with dramatic transitions from an aquatic to a terrestrial life stage. Because optimum phenology is influenced by local environmental conditions, particularly temperature, phenotypic plasticity could play an important role in adaptation to seasonally variable environments. Here, we used a 18-generation longitudinal field dataset from a wild insect (the damselfly Ischnura elegans) and show that phenology has strongly advanced, coinciding with increasing temperatures in northern Europe. Using individual fitness data, we show this advancement is most likely an adaptive response towards a thermally-dependent moving fitness optimum. These field data were complemented with a laboratory experiment, revealing that developmental plasticity to temperature quantitatively matches the environmental dependence of selection and can explain the observed phenological advance. We expand the analysis to the macroevolutionary level, using a public database of over 1 million occurrence records on the phenology of Swedish damselfly and dragonfly species. Combining spatiotemporally matched temperature data and phylogenetic information, we estimated the phenological reaction norms towards temperature for 49 Swedish species. We show that thermal plasticity in phenology is more closely aligned with local adaptation for odonate species that have recently colonized northern latitudes, whereas there is more mismatch at lower latitudes. Our results show that phenological plasticity plays a key role in microevolutionary adaptation within in a single species, and also suggest that such plasticity may have facilitated post-Pleistocene range expansion at the macroevolutionary scale in this insect clade. Impact StatementOrganisms with complex life cycles must time their life-history transitions to match environmental conditions favorable to survival and reproduction. The timing of these transitions - phenology - is therefore of critical importance, and phenology a key trait in adaptive responses to climate change. Here, we use field data from a single species and phylogenetic comparative from over 1 million individual damselfly and dragonfly records to show that plasticity in phenology underlies adaptation at both the microevolutionary scale (across generations in a single species) and the macroevolutionary scale (across deep time in a clade). Our results indicates that phenotypic plasticity has the potential to explain variation in phenology and adaptive response to climate change across disparate evolutionary time scales.