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Bridle, J.

Publications and source records attributed to Bridle, J..

7 recordsLinked to original sources

Evidence from the field that multiple processes maintain hidden adaptive capacity to a novel environment in a wild daisy

Populations often persist in novel environments despite predictions that adaptive capacity to such conditions should be limited by a lack of genetic variation. A leading hypothesis is that genetic variation for adapting to novel environments is maintained but remains hidden under native conditions. However, direct evidence for the mechanisms that maintain this adaptive potential in natural populations is scarce. Here, we integrate data from four large-scale field experiments to test whether variation in selection across life history and environments, together with genetic architecture, maintains genetic variation important for adapting to novel environments. Using a quantitative genetic breeding design, we generated families of the Sicilian daisy, Senecio chrysanthemifolius (Asteraceae), and planted seeds and cuttings across native and novel elevations on Mount Etna. We tracked fitness across elevations, life stages, seasons and generations. Genotypes with higher survival and flowering success at the novel elevation increased adaptive potential, but were only weakly selected against in the native environment where they had slightly lower fitness at a later life-history stage. A negative genetic correlation in seedling survival across seasons indicated that different genotypes were favoured across temporal variation in native environments. Crosses between genotypes with low and high fitness in the novel environment revealed that genotypes that increased adaptive potential had heritable effects on plasticity and fitness across generations, but were recessive and therefore largely hidden in heterozygotes. Together, these results provide rare field-based evidence that weak selection in native environments, temporal variation in selection and dominance effects act together to maintain cryptic adaptive potential in natural populations.

evolutionary biology↗

Temperature and Ultraviolet Radiation Drive Divergent Visible and Near-Infrared Reflectance Patterns in Butterflies

O_LIClimate change poses extreme risks to biodiversity, threatening the ecosystems upon which humanity depends. Understanding the traits that mediate how organisms respond to climatic gradients in space and time will enable better predictions of the taxa and ecological communities most at risk from warming. C_LIO_LIIn insects, colouration influences thermoregulation, but warming responses must be traded off against other selective pressures. We hypothesise that butterfly wing reflectance in visible and near-infrared (NIR) spectra respond differently to temperature and ultraviolet radiation over space and time. We combined existing reflectance data of 97 butterfly species in both NIR and visible wavelengths, with long-term abundance monitoring data of 120 butterfly communities sampled across 1650 m altitude gradients from May to August in two time periods (2004/5 and 2017). C_LIO_LIThe visible and NIR reflectances of butterfly communities showed a non-linear relationship with altitude, with the lowest reflectance (darkest butterflies) at the coolest, highest sites. In contrast, community visible reflectance decreased through the year as temperatures warmed over spring-summer, whereas community NIR reflectance remained constant, revealing divergent responses of reflectance types to seasonal changes. Temperature had opposing effects on visible and NIR reflectance of butterfly communities, where increasing temperature reduced community visible reflectance strongly while increasing community NIR reflectance slightly. C_LIO_LIConsidering the effects on reflectance of shared evolutionary history in a Bayesian hierarchical model for individual species, lighter-coloured (more reflective) species were associated with warmer temperatures - flying later in spring-summer or at lower altitudes. However, instead of decreasing in reflectance through the year and across temperature gradients, species instead became lighter, we expect as a result of a Simpsons paradox. C_LIO_LIThese results emphasise how visible and NIR reflectance wavelength bands mediate butterflies responses to environmental gradients in distinct ways, despite being highly correlated across species. We also show that incorporating phylogeny into trait-environment models is essential; relying on traits alone would lead to incorrect inferences and predictions of taxa most at risk from warming climates. C_LI

ecology↗

Does mother know best? Range-wide narrowing of host preference in Aricia agestis confers fitness benefits but may incur long-term costs

Biological communities are responding to changes in climate through a combination of range shifts and evolution in situ. However, even in systems where we have genomic and phenotypic evidence of recent adaptation, the ecological and fitness consequences of such evolutionary change remain underexplored, especially in terms of consequences for interactions between species. European Lepidoptera are excellent systems for understanding such shifts, given our exceptional knowledge of their ecology, natural history, and past distributions. The UK Brown Argus butterfly (Aricia agestis) has expanded rapidly northward in response to climate change. This expansion has been associated with evolutionary shifts in maternal host preference, from the chalkland restricted but locally common perennial Rockrose (Helianthemum nummularium) to more broadly distributed, but locally rare annual Geraniums (Geraniaceae). Such a rapid range shift offers an excellent opportunity to test how the evolution of novel biotic interactions associated with climate adaptation affects individual fitness and population resilience. Using common garden assays of host preference on females sampled across the UK in 2013 and 2023, we show for the first time that female preference for Geranium molle or Rockrose hosts vary among individuals within as well as among sites and to different extents at different locations. This variation is consistent with genomic signals of recent selective sweeps on these traits. In particular, we show that in 2013, females in the new part of the range are more likely to oviposit on the locally dominant host, while females from the ancestral range will use both hosts, regardless of the locally dominant host. We also demonstrate a significant temporal shift in behaviour, with a narrowing of host preference towards Geranium molle recorded in A.agestis ancestral range in 2023. To evaluate the fitness consequences of these shifts in biotic interactions, we assessed larval performance of 1412 larvae from 49 families on both host plants. Irrespective of maternal preference, feeding on Geranium molle hosts conferred higher survival, faster development and larger adult body size under laboratory conditions. These fitness outcomes are likely linked to Geranium molles significantly higher protein: carbohydrate ratio when compared to Rockrose. Moreover, we also found that larvae fed Geranium molle produced adults with elevated mass-independent resting metabolic rates, a rare demonstration that larval diet has lasting metabolic consequences in a wild butterfly. Crucially, we found no evidence of trade-offs between preference and performance: even offspring of females that laid exclusively on Rockrose also performed better on Geranium molle. These results suggest that Geranium molle confers a general performance advantage, enhancing traits likely to promote population persistence where Geranium molle is reliably available. However, despite selection favouring Geranium molle in warming climates, we also show that a narrowing of host preference towards these more widespread host plants throughout the UK range is likely to make A.agestis populations more vulnerable under future warmer, drier conditions, when compared to Rockrose. Together these findings highlight a central challenge in evolutionary biology: what happens when traits that are adaptive in the short term spread rapidly through populations, but are likely to become maladaptive as environmental conditions continue to change?

evolutionary biology↗

Genetic differences in plasticity across environmental scales determine fitness along an ecological gradient

When populations suffer reduced fitness in novel environments, genotypes that better adjust their phenotype to cope with environmental change can aid persistence by reducing the severity of fitness declines. However, we know little about how plastic changes in phenotype allow different genotypes to track environmental variation across ecological gradients, particularly as environments become novel. We transplanted numerous clones of 19 genotypes of a Sicilian daisy, Senecio chrysanthemifolius, at four elevations on Mt Etna. We assessed fitness at native and novel elevations and quantified leaf plasticity among and within elevations. Genotypes with higher fitness at novel elevations showed lower variance in fitness, lower plasticity across elevations, but higher plasticity within elevations compared to those with higher fitness in the native range. Our results suggest that there are genotypes hidden in a population whose plasticity better tracks novel environmental variation at multiple scales, which will be crucial for population persistence under rapid environmental change.

evolutionary biology↗

The evolution of novel biotic interactions at ecological margins in response to climate change involves alleles from across the geographical range of the UK Brown Argus butterfly

Understanding the rate and extent to which populations can adapt to novel environments at their ecological margins is fundamental to predicting the persistence of biological communities during ongoing and rapid global change. Recent range expansion in response to climate change in the UK butterfly Aricia agestis is associated with the evolution of novel interactions with a larval food plant, and the loss of its ability to use its ancestral larval host species. Using ddRAD analysis of 61210 variable SNPs from 261 females from throughout the UK range of this species, we identify genomic regions at multiple chromosomes that are associated with these evolutionary responses, and their association with demographic history and ecological variation. Gene flow appears widespread throughout the range, despite the apparently fragmented nature of the habitats used by this species. Patterns of haplotype variation between selected and neutral genomic regions suggest that evolution associated with climate adaptation is polygenic, resulting from the independent spread of existing alleles throughout the established range of this species, rather than the colonisation of pre-adapted genotypes from coastal populations. These data suggest that rapid responses to climate change do not depend on the availability of pre-adapted genotypes. Instead, the evolution of novel forms of biotic interaction in Aricia agestis has occurred during range expansion, through the assembly of novel genotypes from alleles from multiple localities.

evolutionary biology↗

Climate-driven variation in biotic interactions provides a narrow and variable window of opportunity for an insect herbivore at its ecological margin

Climate-driven geographic range shifts have been associated with transitions between dietary specialism and generalism at range margins. The mechanisms underpinning these often transient niche breadth modifications are poorly known, but utilisation of novel resources likely depends on phenological synchrony between the consumer and resource. We use a climate-driven range and host shift by the butterfly Aricia agestis to test how climate-driven changes in host phenology and condition affect phenological synchrony, and consider implications for host use. Our data suggest that the perennial plant which was the primary host before range expansion is a more reliable resource than the annual Geraniaceae upon which the butterfly has become specialised in newly colonised parts of its range. In particular, climate-driven phenological variation in the novel host Geranium dissectum generates a narrow and variable window of opportunity for larval productivity in summer. Therefore, although climatic change may allow species to shift hosts and colonise novel environments, specialisation on phenologically-limited hosts may not persist at ecological margins as climate change continues. We highlight the potential role for phenological (a)synchrony in determining lability of consumer-resource associations at range margins, and the importance of considering causes of synchrony in biotic interactions when predicting range shifts.

ecology↗

Molecular analyses reveal consistent food web structure with elevation in rainforest Drosophila - parasitoid communities

The analysis of interaction networks across spatial environmental gradients is a powerful approach to investigate the responses of communities to global change. Using a combination of DNA metabarcoding and traditional molecular methods we built bipartite Drosophila-parasitoid food webs from six Australian rainforest sites across gradients spanning 850 m in elevation and 5{degrees} Celsius in mean temperature. Our cost-effective hierarchical approach to network reconstruction separated the determination of host frequencies from the detection and quantification of interactions. The food webs comprised 5-9 host and 5-11 parasitoid species at each site, and showed a lower incidence of parasitism at high elevation. Despite considerable turnover in the relative abundance of host Drosophila species, and contrary to some previous results, we did not detect significant changes to fundamental metrics of network structure including nestedness and specialisation with elevation. Advances in community ecology depend on data from a combination of methodological approaches. It is therefore especially valuable to develop model study systems for sets of closely-interacting species that are diverse enough to be representative, yet still amenable to field and laboratory experiments.

ecology↗