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

我的研究计划的长期目标是了解在复杂的生物系统中新颖的特征是如何产生和多样化的。这是进化生物学的一个核心问题，100多年来一直没有得到解决。我的研究项目处于新兴领域Eco-Evo-Devo的前沿，该领域整合了传统上独立的生态学、进化论和发育生物学领域。该领域的一个主要焦点是了解基因和环境在发育过程中如何相互作用以产生新的特征，以及这些特征随后如何在其生态环境中多样化。我们关注蚂蚁的一个关键形态特征——工蚁阶层——它的起源和多样化加强了它们的劳动分工，从而促进了它们在生态和进化上的成功。我将利用最近的几个发现，这些发现已经开始揭示新的工蚁阶级是如何在蚂蚁进化的三个主要形态转变中产生的。这些转变标志着蚂蚁社会复杂性的逐步增加，这始于(1)群居性（真正的社会行为）的起源；其次是(2)“不归点”（当社会性变得不可逆转时，因为工人的生殖能力显著降低）；最后(3)单一工人阶层的多样化，形成了一个由形态和行为上的子阶层组成的复杂系统。在接下来的五年里，我们将启动3个项目，旨在了解蚂蚁进化中3个主要转变背后的发育机制。这3个项目将采用Eco-Evo-Devo的综合方法（分子和发育生物学、内分泌学、基因组学、田野调查、人口和比较生物学和行为学）：

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.