A synthetic synthesis to explore animal evolution and development

Abstract

Identifying the general principles by which genotypes are converted into phenotypes remains a challenge in the post-genomic era. We still lack a predictive understanding of how genes shape interactions among cells and tissues in response to signalling and environmental cues, and hence how regulatory networks generate the phenotypic variation required for adaptive evolution. Here, we discuss how techniques borrowed from synthetic biology may facilitate a systematic exploration of evolvability across biological scales. Synthetic approaches permit controlled manipulation of both endogenous and fully engineered systems, providing a flexible platform for investigating causal mechanisms in vivo . Combining synthetic approaches with multi-level phenotyping (phenomics) will supply a detailed, quantitative characterization of how internal and external stimuli shape the morphology and behaviour of living organisms. We advocate integrating high-throughput experimental data with mathematical and computational techniques from a variety of disciplines in order to pursue a comprehensive theory of evolution. This article is part of the theme issue ‘Genetic basis of adaptation and speciation: from loci to causative mutations’.

Rapid response of fly populations to gene dosage across development and generations

“…Importantly, these observations highlight the deep connections between multiple phenotypic layers of multicellular systems and argue for a broader ‘phenomics’ perspective (Gandara et al, 2022), instead of a strictly gene-centric view. In the future, exploring the interplay of metabolic and developmental networks could transform our understanding of evolution and development across variable ecologies (Miyazawa and Aulehla, 2018; Perkins et al, 2022), as such processes are fundamentally linked (White et al, 2022).…”

“…Thousands of individual genes may contribute to phenotypes through expression in relevant cells (Boyle et al, 2017), and the contributions of each genetic variant to developmental fates are often small and challenging to measure (Frankel et al, 2011; Wood et al, 2014; Yengo et al, 2018). Therefore, it is essential to consider regulatory evolution and development both at the systems level and across populations (Gandara et al, 2022; Houle et al, 2010; Perkins et al, 2022). Clearly, approaches to elicit the relationships between different phenotypic layers and how these changes manifest across populations are needed to understand the evolution of developmental regulatory networks.…”

Interdisciplinary approaches to predicting evolutionary biology

“…Advances in genome sequencing are providing unprecedented insights into biological mechanisms and evolutionary processes. From massively parallel evolution experiments, high-throughput sequencing and large-scale phenotypic assays, we now have an unprecedented amount of empirical evolutionary information [ 4 ]. New genome editing approaches are opening up new experimental avenues no longer limited by ‘chance’ [ 5 ], and these approaches allow us to empirically describe and quantify the types of phenotypic variation generated by genetic variation.…”

Genetic basis of speciation and adaptation: from loci to causative mutations

“…Using systematic synthetic biology approaches (e.g. Crocker et al [ 90 ] in this issue), it is now possible to artificially generate multiple genotypes that do not exist in natural populations and to investigate the evolvability and constraint of evolution.…”