Chapter 1
Introduction to Evo-Devo-Anthro

Campbell Rolian1 and Julia C. Boughner2

1 Faculty of Veterinary Medicine, University of Calgary, Calgary, AB, Canada

2 Department of Anatomy and Cell Biology, College of Medicine, University of Saskatchewan, Saskatoon, SK, Canada

Evolutionary developmental biology, or evo-devo, is a relatively young branch of biology concerned with how and why organismal development matters to evolution. Evo-devo encompasses a range of unified research questions and empirical approaches that can be grouped into two complementary research areas (Laublicher 2007). The first area concerns the process of organismal development. This research uses molecular tools such as studies of gene and protein expression patterns to understand how processes of organismal development have evolved and produced phenotypic diversification at macroevolutionary scales. The second approach focuses on the role that process plays in structuring the pattern of heritable phenotypic variation among individuals. This approach relies on quantitative genetic theory and morphometric tools to measure developmentally determined patterns of phenotypic variation, typically at the level of populations, and to understand how these patterns have biased or constrained the rate and direction of evolutionary change within and between species (Raff 2000).

In the past couple of decades, the types of research questions that evo-devo addresses have also become of great interest to biological anthropologists. The discipline is gaining traction among researchers interested in the role(s) played by organismal development in the evolution of uniquely human, and non-human primate, traits. This volume aims to provide an overview of past and ongoing research in evo-devo specifically as it applies to the study of human and primate evolution - Evolutionary Developmental Anthropology (EDA, or Evo-Devo-Anthro). In this introductory chapter, we begin with a brief survey of the origins and principal discoveries of evolutionary developmental biology. We then discuss the emergence of evo-devo in anthropology in the context of past research at the interface of human/primate development and evolution. Finally, we summarize the current state of affairs in the growing field of evo-devo anthropology, and highlight a number of knowledge gaps which are promising avenues for future research in this field.

A Brief History of Evo-Devo

As this volume attests, many different approaches to studying the reciprocal interactions of development and evolution fall under the broad umbrella of evolutionary developmental biology. As a result, finding consensus on a single definition of evo-devo that describes what the field is, and what it seeks to accomplish, can be challenging. The lack of consensus stems from two distinct goals: studying process at macro- and microevolutionary scales. These goals are driven by the desire to understand the broad developmental processes that drive the evolution and diversification of form among species and higher taxonomic levels, versus the lower level (but likely similar) processes that pattern the structure of phenotypic variation among individuals within populations, as the fuel for natural selection. This lack of consensus on what evo-devo is also stems from the fact that, although it is in some ways a "new" discipline (Carroll 2005), its roots run deep. The study of organismal development, evolutionary processes, and their complex interactions is at least 150 years old, dating back to 19th-century evolutionary embryologists such as Ernst Haeckel and Francis Balfour, and to Charles Darwin himself (Hall 1999). These pioneers focused on the comparative study of embryology as a window into organismal development, and were particularly interested in what these processes could reveal across taxa about phylogenetic relationships and the evolution of specific traits with a shared evolutionary origin but different morphologies and functions (i.e., homologies such as the hands of dolphins, bats, and humans) (Hall 1999; Maienschein 2007).

Many of these early studies in comparative embryology were concerned with comparing patterns of growth and development within and among species. These now-classic works inferred that differences in ontogenetic patterns must account for variation within populations, but especially morphological divergence among taxa in deep time. Evolutionary embryologists were less concerned with lower level biological processes (i.e., cellular dynamics) that would explain described developmental patterns across all vertebrates. This was largely a practical issue: describing macroscopic changes in vertebrate fetal development between taxa was considerably simpler than documenting changes in the spatial relationships of cells and tissues during morphogenesis. Productivity in this area of study has since increased dramatically with the advent and benefit of modern molecular tools.

In contrast to other fields in biology such as population genetics, progress in embryology for much of the 20th century was relatively slow, in part due to the technical challenges associated with studying embryonic development, to the extent that the discipline contributed relatively little to the modern evolutionary synthesis of the 1940s (Carroll 2005; Maienschein 2007). The Modern Synthesis united several disciplines studying evolutionary biology from different angles, particularly population genetics and paleontology (Mayr and Provine 1998). It suggested that the evolution of quantitative traits is gradual, and occurs through mechanisms consistent with Mendelian genetics, namely through small genetic changes that produce continuous (i.e., bell-curved) variation within populations, which can then be acted upon by selective forces. Proponents further argued correctly that this process, occurring at the population level (microevolution), could be extrapolated to higher taxonomic levels and longer timescales to explain macroevolutionary patterns.

Despite the realization that development interposes itself between genes and phenotypes, and hence likely influences the transition from one to the other, the study of embryology was not revived after the synthesis. Rather, the synthesis served to affirm the primacy of genes and phenotypes in determining evolutionary change, relegating organismal development, not to mention the field of epigenetics (sensu Waddington, Jamniczky et al. 2010) to a secondary, less important, process linking genes to phenotypes. For several decades following the synthesis, organismal development continued to be viewed as a black box, something that was "hopelessly complex and would involve entirely different explanations for different types of animals" (Carroll 2005:6). However, the reasons for ignoring organismal development in the study of the evolution of animal form, in particular early embryological events such as morphogenesis, were not entirely philosophical. Considerable practical obstacles in developmental biology remained: although genes were now seen as primary drivers of evolutionary change, prior to the late 1970s no one had successfully identified and localized genes that determine animal form, let alone how changes in their structure or function could lead to the evolution of animal form and function.

Breakthroughs in developmental biology were finally achieved in the late 1970s and 1980s, first in fruit flies, and eventually in vertebrates. These breakthroughs were rooted in technological innovations in molecular genetics: especially the ability to identify, localize, and manipulate genes physically; in particular to visualize their expression patterns; and to relate these to temporal and spatial effects on the development of organismal form (for example through gene inactivation) (Anderson and Ingham 2003). Homeotic genes were among the first genes shown to control key aspects of development, and some consider their discovery to mark the birth of evo-devo (Hall 1999; Carroll 2005). Homeotic genes regulate segmental patterning in the metazoan embryo. Early analyses revealed that loss-of-function mutations in these genes in Drosophila caused segmental identity shifts (homeotic transformations), where one segment along the embryo's anterior-posterior axis would take on the likeness of an adjacent segment (Lewis 1978). Homeotic genes act as transcription factors, proteins that regulate the transcriptional activity of other genes (Mallo et al. 2010).

Soon after their discovery in Drosophila, similar genes with similar tasks in embryonic patterning were uncovered in vertebrates, including humans (Tournierlasserve et al. 1989; Krumlauf 1994). These discoveries led to a fundamental evo-devo concept: the developmental genetic toolkit (Carroll et al. 2005). Toolkits describe subsets of genes that specify animal form during embryological development. Toolkit genes are distinct from those involved in the routine functions of all cells (housekeeping genes, Zhu et al. 2008), and those that are uniquely expressed in differentiated cell types. Toolkit genes belong to signalling pathways, many acting as transcription factors that regulate the activities of other genes that specify cell fates and/or establishing spatial and temporal expression patterns during morphogenesis. The same toolkits are recruited several times during an individual's development, and contribute to the development of vastly different structures. As a result, toolkit...