Modularity in animal development and evolution: Elements of a conceptual framework for EvoDevo

Abstract

For at least a century biologists have been talking, mostly in a black-box sense, about developmental mechanisms. Only recently have biologists succeeded broadly in fishing out the contents of these black boxes. Unfortunately the view from inside the black box is almost as obscure as that from without, and developmental biologists increasingly confront the need to synthesize known facts about developmental phenomena into mechanistic descriptions of complex systems. To evolutionary biologists, the emerging understanding of developmental mechanisms is an opportunity to understand the origins of variation not just in the selective milieu but also in the variability of the developmental process, the substrate for morphological change. Ultimately, evolutionary developmental biology (EvoDevo) expects to articulate how the diversity of organic form results from adaptive variation in development. This ambition demands a shift in the way biologists describe causality, and the central problem of EvoDevo is to understand how the architecture of development confers evolvability. We argue in this essay that it makes little sense to think of this question in terms of individual gene function or isolated morphometrics, but rather in terms of higher-order modules such as gene networks and homologous characters. We outline the conceptual challenges raised by this shift in perspective, then present a selection of case studies we believe to be paradigmatic for how biologists think about modularity in development and evolution.

Developmental dynamics of the bronchial (airway) and air sac systems of the avian respiratory system from day�3 to day 26 of life: a scanning electron microscopic study of the domestic fowl, Gallus gallus variant domesticus

“…It is becoming acutely imperative for developmental biologists to seek to underpin and translate known facts of development into sound, conceptually easy, mechanistic descriptions that meaningfully explain the natural processes that decree and secure morphological novelty. Synthesis of phylogenetic parameters with developmental aspects now constitutes the "evolutionary-developmental biology approach" that has been termed EvoDevo (Gilbert et al 1996;Dassow and Munro 1999), a highly powerful means of explicating the essence of organic, systemic, and organismal adaptive design. Nearly a century ago, Locy and Larsell (1916a) pointed out that "the avian lung exhibits a special architecture and upon our understanding of this architecture will depend our conception of its physiology".…”

Head, Body and Fins: Patterns of Morphological Integration and Modularity in Fishes

“…Organisms are hypothesized to be constructed from distinct sub-units termed modules that are highly integrated internally and behave quasi-independently during ontogeny and evolution (Wagner 1996;von Dassow and Munro 1999;Hansen et al 2003;Klingenberg et al 2003;Wagner et al 2007;Kuratani 2009). Modularity is tightly linked to the concept of morphological integration, which postulates that functionally or developmentally related traits should form highly cohesive morphological units (Olson and Miller 1958;Cheverud 1982;Zelditch 1987;Cheverud 1996;Chernoff and Magwene 1999).…”

Body-form Evolution in the Scincid Lizard Clade Lerista and the Mode of Macroevolutionary Transitions

“…Modular organisation is a pervasive feature of organismal development, and an understanding of the consequences of developmental modularity for phenotypic evolution is considered by many authors as fundamental to a conceptual synthesis of developmental and evolutionary biology (e.g., Raff 1996;Wagner and Altenberg 1996;von Dassow and Munro 1999;Bolker 2000;Schlosser 2002;West-Eberhard 2003;Schlosser 2004;Schlosser and Wagner 2004). Modules of development are integrated, quasi-autonomous systems that contribute to ontogeny, and include transcriptional regulation mechanisms (incorporating particular cis-regulatory elements and transcription factors, and the basal transcriptional apparatus), signalling cascades, gene regulatory networks, specific cell types, and organ primordia (Schlosser 2004).…”