How a growing organismal perspective is adding new depth to integrative studies of morphological evolution

Abstract

Over the past half century, the field of Evolutionary Developmental Biology, or Evo-devo, has integrated diverse fields of biology into a more synthetic understanding of morphological diversity. This has resulted in numerous insights into how development can evolve and reciprocally influence morphological evolution, as well as generated several novel theoretical areas. Although comparative by default, there remains a great gap in our understanding of adaptive morphological diversification and how developmental mechanisms influence the shape and pattern of phenotypic variation. Herein we highlight areas of research that are in the process of filling this void, and areas, if investigated more fully, that will add new insights into the diversification of morphology. At the centre of our discussion is an explicit awareness of organismal biology. Here we discuss an organismal framework that is supported by three distinct pillars. First, there is a need for Evo-devo to adopt a high-resolution phylogenetic approach in the study of morphological variation and its developmental underpinnings. Secondly, we propose that to understand the dynamic nature of morphological evolution, investigators need to give more explicit attention to the processes that generate evolutionarily relevant variation at the population level. Finally, we emphasize the need to address more thoroughly the processes that structure variation at micro- and macroevolutionary scales including modularity, morphological integration, constraint, and plasticity. We illustrate the power of these three pillars using numerous examples from both invertebrates and vertebrates to emphasize that many of these approaches are already present within the field, but have yet to be formally integrated into many research programs. We feel that the most exciting new insights will come where the traditional experimental approaches to Evo-devo are integrated more thoroughly with the principles of this organismal framework.

Co-opting evo-devo concepts for new insights into mechanisms of behavioural diversity

“…Developmental plasticity and robust developmental processes together allow for the integrated effects of individual mutations on mechanisms that contribute to behavioural outcomes, as one change can have cascading consequences on all levels of biological organisation. As was urged for morphological studies (Sanger and Rajakumar, 2019), we encourage researchers to characterize the molecular, cellular and developmental mechanisms that translate genetic variation into behavioural variation at the population level. Understanding these developmental cascades may reveal which mechanistic changes are key innovations in a lineage and how ancestral developmental processes structure behavioural variation.…”

“…Evo-devo research includes both macroevolutionary comparisons of developmental genetics and population-level analyses. Macroevolutionary comparisons can identify modifications of ancestral developmental programs that give rise to evolutionary innovations, whereas population-level analyses can reveal developmental influences on the structure of morphological variation and covariation among phenotypes (Box 1; reviewed in Sanger and Rajakumar, 2019). Relevant to both macroevolutionary comparisons and populational analysis is understanding how phenotypic variation is generated.…”

Embryonic development of a parthenogenetic vertebrate, the mourning gecko (Lepidodactylus lugubris)

“…Robust phylogenetic analysis, genomic information, and detailed developmental data are critical tools to investigate the origins of morphological novelty and convergence. Ideally, by employing a model clade approach, an integrated comparison between closely related taxa with variable phenotypes allows for polarization of ancestral character states and fine‐scale investigations into morphological evolution and development . By including another gecko species to the growing number of squamate embryonic staging series, we hope to promote model clade approaches to squamate and vertebrate evo‐devo.…”

“…Ideally, by employing a model clade approach, an integrated comparison between closely related taxa with variable phenotypes allows for polarization of ancestral character states and fine-scale investigations into morphological evolution and development. 105 By including another gecko species to the growing number of squamate embryonic staging series, we hope to promote model clade approaches to squamate and vertebrate evo-devo. For example, comparative squamate evo-devo studies that include a gecko and any other non-gekkotan squamate species allow the investigators to sample the phylogenetic breadth of squamates.…”

Embryonic and larval development of the northern pike: An emerging fish model system for evo‐devo research

“…However, the notable absence of a comprehensive developmental staging table has limited the use of the northern pike. Here, we provide a description of embryonic and larval stages that, together with the already available genomic and transcriptomic resources (Rondeau et al, ; Sanger & Rajakumar, ), lays a strong foundation for the wider adoption of this powerful research organism. The present study provides the first reliable staging table of the northern pike, from the one‐cell stage to the first dermal bones of free‐swimming juveniles, supplemented with histological details of embryonic tissues (summarized in Table , Figures and ).…”