Search bioRxiv⌕ Search

bioRxiv · 10.1101/269175

On the timing of bill length evolution in British great tits: A comment on Bosse et al. 2017.

Abstract

Long-term field studies coupled with quantitative genomics offer a powerful means to understand the genetic bases underlying quantitative traits and their evolutionary changes. However, analyzing and interpreting the time scales at which adaptive evolution occurs is challenging. First, while evolution is predictable in the short term, with strikingly rapid phenotypic changes in data series, it remains unpredictable in the long term. Second, while the temporal dynamics of some loci with large effect on phenotypic variation and fitness have been characterized, this task can be complicated in cases of highly polygenic trait architecture implicating numerous small effect size loci, or when statistical tests are sensitive to the heterogeneity of some key characteristics of the genome, like recombination rate variations. After introducing these aforementioned challenges, we discuss a recent investigation of the genomic architecture and spatio-temporal variation in great tit bill length, which was related to the recent use of bird feeders. We discuss how this case study illustrates the importance of considering different temporal scales and evolutionary mechanisms both while analyzing trait temporal trends and when searching for and interpreting the signals of putative genomic footprints of selection. More generally this commentary discusses interesting challenges for unraveling the time scale at which adaptive traits evolve and their genomic bases.\n\nImpact summaryAn important goal in evolutionary biology is to understand how individual traits evolve, leading to fascinating variations in time and space. Long-term field studies have been crucial in trying to understand the timing, extent, and ecological determinants of such trait variation in wild populations. In this context, recent genomic tools can be used to look for the genetic bases underlying such trait variation and can provide clues on the nature and timing of their evolution. However, the analysis and the interpretation of the time scales at which evolution occurs remain challenging. First, analyzing long-term data series can be tricky; short-term changes are highly predictable whereas long-term evolution is much less predictable. A second difficult task is to study the architecture of complex quantitative traits and to decipher the timing and roles of the several genomic mechanisms involved in their evolution. This commentary introduces these challenges and discusses a recent investigation of the nature and timing of ecological and genomic factors responsible for variation in great tit bill length. Overall, we raise cautionary warnings regarding several conceptual and technical features and limitations when coupling analyses of long-term and genomic data to study trait evolution in wild populations.

Source connections

Explore related subjects

Keep this discovery

Explore connections, maps & timelines

BibTeXRIS

Perrier, C., Charmantier, A.. 2018-02-22. On the timing of bill length evolution in British great tits: A comment on Bosse et al. 2017.. https://doi.org/10.1101/269175

Cite the original work for its findings. Save a collection to share your selection of sources.

KEEP EXPLORING

Related preprints

The pupal stage shapes life-history trade-offs across metamorphosis

Dealing with ecological stressors during development often comes at the expense of later-life performance. Although such trade-offs are well studied as two-stage systems such as larva-adult trade-offs, they are rarely examined across multiple developmental stages, limiting our understanding of how ecological effects are integrated throughout complex life cycles. We addressed this gap using a multistage experimental framework in Aedes aegypti, where we exposed individuals to predation risk during the larval stage, the pupal stage, both stages, or neither, and quantified developmental, physiological, and adult fitness traits. Contrary to expectations, predation risk across successive stages did not produce cumulative fitness costs, and traits varied in their responses. Both males and females emerged faster when exposed to risk, with lighter bodies, but males paid an additional cost of reduced starvation resistance when the pupal stage was exposed. Surprisingly, despite their lower body mass, females showed enhanced reproductive performance when both stages were exposed to risk. Overall, responses were stage- and sex-specific, with exposure during the non-feeding pupal stage imposing greater life-history costs than larval exposure alone. Measurements across the larva-pupa-adult continuum further revealed that traits such as body mass and energy reserves respond differently before and after metamorphosis, highlighting the role of the pupa in mediating trade-offs. Our findings identify the pupal stage as a critical mediator of life-history trade-offs and demonstrate the value of a multistage framework for understanding the role of each stage in life-history evolution.

evolutionary biology↗

Cell-lineage selection interacts with development and life history to shape the rates and identity of heritable mutations

Mutation rates determine the supply of heritable variation and are central to evolutionary theory, yet they are usually treated as properties of molecular mutational processes. We hypothesised that mutation rates are also shaped by selection among cell lineages within organisms and that the strength of this process depends on developmental and life-history traits. To test the extent of this idea, we combined mathematical modelling with experiments in Drosophila melanogaster and treated mutation rates as emergent properties of interactions among molecular mutagenesis, development, life history, and cell-lineage selection. The model predicts that even modest effects of mutations on cellular fitness can substantially alter the probability that mutations are transmitted, and that these effects depend strongly on developmental architecture, germline dynamics, and time to reproduction. In Drosophila, we experimentally demonstrate biased transmission of a mutation affecting cellular proliferation and show that this bias changes over the reproductive lifespan of the individual. Extending the model genome-wide reveals that the cellular distribution of fitness effects and its interaction with developmental parameters influence both the estimated mutation rate and the composition of transmitted mutations, producing transmission biases that favour mutations with particular cellular fitness effects. These results suggest that developmental and life-history parameters determine how cellular fitness effects translate into transmission bias; therefore, estimates of heritable mutational input can vary from species to species even under constant molecular mutagenesis. By filtering mutations before they enter populations, developmental and life-history evolution can modify both the rate and the nature of heritable variation and thereby influence evolutionary trajectories.

evolutionary biology↗

A Deep Phylogenetic Split Between Short- and Long-Wavelength-Tuned Visual Systems in Surgeonfishes (Acanthuridae)

The light environment, coupled with ecology, is widely thought to drive visual adaptation, creating species-specific visual niches. However, coral reef ecosystems experience continuous spatiotemporal variations in light conditions, and mechanisms such as phenotypic plasticity may be essential for coral reef animals to adjust to such changing sensory requirements. It remains unclear how widespread colour vision plasticity is, or the extent to which ecology and phylogeny drive plasticity in coral reef fishes. Using a comparative transcriptomic approach across 22 species, we aimed to investigate visual plasticity within a prominent coral reef fish family, surgeonfishes (Acanthuridae), in response to changes in the light environment throughout development and across seasons in adults. Surprisingly, we uncovered a deep phylogenetic split (~42 mya) in visual opsin gene expression profiles, with Nasinae expressing a shorter-shifted palette than Acanthurinae, which coincides with the divide between water-column and benthic-feeding modalities during the speciation of their last common ancestor. However, opsin gene expression showed little variation in response to seasonal or ontogenetic shifts in the light environment, nor in the broad functional feeding groups extant species from both subfamilies fall under. Thus, the invariable visual gene expression observed in present-day surgeonfishes appears to be dictated by phylogenetic inertia, despite rapid diversification into a range of ecological niches. This suggests that spectral tuning into two main modalities, short and long, reduces the need for visual plasticity, allowing larger and more mobile coral reef fishes to conduct visually guided behaviours across the entire range of light environments they encounter.

evolutionary biology↗