Eco-Evo-Devo and the origin of novelty in complex biological systems

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THE LONG-TERM GOAL OF MY RESEARCH PROGRAM IS TO UNDERSTAND HOW NOVEL FEATURES ORIGINATE AND DIVERSIFY IN COMPLEX BIOLOGICAL SYSTEMS. This a central problem in evolutionary biology that has remained largely unresolved for over 100 years. My research program is on the leading edge of the emerging field of Eco-Evo-Devo, which integrates the traditionally separate fields of ecology, evolution, and developmental biology. A main focus of this field is to understand how genes and environment interact during development to generate novel features and how these features subsequently diversify in their ecological environments. We focus on a key morphological trait in ants – the worker caste – whose origin and diversification has enhanced their division of labor, and consequently, their ecological and evolutionary success. I will capitalize on several recent discoveries that have started to uncover how novel worker castes originated during 3 major morphological transitions in ant evolution. These transitions mark the progressive increase in complexity of ant societies beginning with (1) the origin of eusociality (true social behavior); followed by (2) the ‘point of no return’ (when eusociality becomes irreversible because the reproductive capacity of workers is significantly reduced); and culminating in (3) the diversification of a single worker caste into a complex system of morphological and behavioral subcastes. Over the next five years, we will initiate 3 projects that aim to understand the developmental mechanisms underlying 3 major transitions in ant evolution. These 3 projects will use the integrative approaches of Eco-Evo-Devo (molecular and developmental biology, endocrinology, genomics, fieldwork, population and comparative biology and behavior): PROJECT 1: Origin of Eusocially: this major transition is associated with the origin of wing polyphenism, where a single genome evolves the ability to produce winged queens or wingless workers in a single colony in response to environmental cues. We will build on 10 years of research in my lab to test whether this transition occurred through key nodes in the networks controlling wing development. PROJECT 2: The ‘Point of No Return:’ we recently discovered molecular defects in worker ovaries that enhance social harmony by reducing the reproductive capacity of workers. We will test whether these defects are regulated by increased activity of “transposable elements” in workers via the inactivation of a developmental pathway in response to social cues. PROJECT 3: Origin of Novel Worker Subcastes: we recently discovered that wing vestiges, which appear during larval development in the wingless worker caste, are not useless organs but have acquired a new developmental function ¬– they are signaling centers that regulate head and body size of workers. We will test whether novel subcastes have originated and diversified through this new function.