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Effects of climate change on adult body size: Towards an integrative approach to understand the underlying mechanisms, the consequences across the lifespan, and improve our predictive ability

Periodic Reporting for period 2 - CLIMGROWTH (Effects of climate change on adult body size: Towards an integrative approach to understand the underlying mechanisms, the consequences across the lifespan, and improve our predictive ability)

Okres sprawozdawczy: 2023-03-01 do 2024-02-29

Changes in adult body size have become a flagship response to climate change. In organisms with a finite growth, as mammals and birds (higher vertebrates), it is thought to result foremost from climate-induced changes in growth trajectories (plasticity) rather than from changes in the frequency of alleles coding for body size (microevolution). Quantifying the relative contributions of these two mechanisms is, however, fundamental to be able to predict the speed of responses to climate changes and the ability of species to adapt to these changes in the long term. These knowledge gaps were addressed by combining complex, state-of-the-art, statistical modelling approaches: (1) testing for the first time in a higher vertebrate the contribution of developmental plasticity and microevolution at accounting for a change in body size in response to climate change using pedigree-based quantitative genetic models; (2) providing long-awaited results on the lifelong consequences of natal climatic conditions on individual life histories, (3) their transgenerational effects on offspring life histories; and (4) addressing the debate between quantitative geneticists and demographers in how to generate reliable predictions for responses to climate change by applying the different approaches in the same study system.
This project provides the first evidence of microevolutionary changes in size in a vertebrate in response to climate change, of the lifelong effects of the growing condition and of the effects on individual fitness of these changes in size.
This project relied on an unprecedented individual-based long-term database (>4,000 individuals, >20 years) collected in a Swiss population of Alpine swifts by the return-phase host, Dr Bize. The Alpine swift is the perfect study species, as it presents outstanding morphological and metabolic characteristics (non-stop flights of up to 200 days), and preliminary results showed a significant increase in body size. The long-term dataset and ongoing monitoring of this bird species is now managed by the Swiss Ornithological Institute under the leadership of the return-phase host. The project aimed at answering 4 questions or Research Objectives (ROs).

RO1: Is phenotypic change mostly driven by plasticity or by microevolution?
RO2: What are the lifelong consequences of early-life climate conditions?
RO3: Is there evidence for transgenerational effects of natal climatic conditions?
RO4: So, who is right: quantitative geneticists or demographers?

The overarching aim of this project was to explain what drives the increase in size of adult Alpine swifts over the past 20 years. Four morphological traits swifts (wings, tail, sternum and body mass) were investigated. First, by using a within-individual centring approach, it was shown that the increase in wing and tail length of adult swifts was explained by the selective recruitment of bigger individuals over the years and by a within-individual increase in size over the first years after recruitment. Second, using quantitative genetic modelling (multi-trait animal models in a Bayesian framework), it was shown that all traits were heritable, and thus could respond to selection, and that the presence of strong genetic correlations between wing and tail length could explain their joined response. Finally, an indication that microevolution is happening in our population was discovered by analysing the breeding values extracted from my quantitative genetic models.

These traits' heritability, genetic correlation and breeding values at the nestling stage were investigated using again multi-trait animal models. Results show that, as in adults, nestling traits are generally heritable and genetically correlated. In particular, wings have been growing faster, and chicks fledge with longer wings at the genotypic level. This has long-term consequences on their probability of recruitment, shaping the population of breeding adults. In particular, birds with longer wings are recruited more in recent years.

The effects of early-life weather conditions on the growth, size at fledging and survival up to fledging of the nestlings were investigated using GLMMs together with the R package climwin to investigate the effects of weather. This package allows the identification of the most important weather parameters and the time period in which they affect the trait of interest.

Overview of the main results:
Climate has significant effects on the wing growth of nestlings, and nestlings have grown their wings faster in recent decades, which is linked with an earlier age at fledging. Selection on nestling wing length over the years, as fewer and fewer nestlings with shorter wings were recruited as breeders in the population. Adult birds showed increased wing and tail length but not body mass or sternum. Within-individual centring models show that these changes were explained by demographic effects, with new recruits (especially females) having longer wings and tails over the years (no change in recruitment age), and by plasticity, with individuals moulting and growing longer feathers over the first few years after recruitment. All adult and nestling traits were heritable, with genetic correlations among most of them, and we found evidence of microevolution in wing length. Indeed, both developmental plasticity and microevolution are both driving the observed changes in adult and nestling body size in response to climate change. Adult females with longer wings are also able to produce more eggs and more fledglings throughout their lives. Our study highlights the importance of plasticity in explaining changes in adult shape and provides an insightful explanation of trait evolutionary constraints.

Dissemination of the results:
The different results of this project should lead to the publication of at least four scientific articles. The results were also disseminated to a large audience in Ecology and Evolution through presentations at two national and two international conferences, five invited seminars at universities, and one symposium on phenotypic adaptations to climate change. Three invited talks were also given to a large general public audience.
At the end of CLIMGROWTH, we are able to understand and predict with an unprecedented level of detail how a species responds to climate change. This has been achieved by using a carefully selected free-living species that is ideally suited for this project, and by combining complex, state-of-the-art, statistical modelling approaches in order to (i) test for the first time in a higher vertebrate the contribution of developmental plasticity and microevolution at accounting for a change in body size in response to climate change (RO1); (ii) provide long-awaited results on the consequences of climate change on individuals across their lifespan (RO2), both within and between generations (RO3); and report on what is the best modelling approach to predict response to climate change (RO4). CLIMGROWTH has tackled several challenges few have dealt with before within a single research program, such as modelling genetic correlation across morphometric traits to account for evolutionary constraints in response to selection, measuring selection at different life stages to account for the ‘invisible fraction’, and applying alternative but complementary modelling approaches to predict responses to climate change.
The researcher Giulia Masoero holding an Alpine swift, her study species.