We are eco-evo-devo ...
We are in the midst of a conceptual revolution in the biological sciences as the traditional borders between ecology, developmental and evolutionary biology are breaking down. The general goal of research in the Abouheif lab is to integrate these fields to understand how genes and environment interact during development (see figure below), and how this interaction influences the evolution of complex biological systems.
From Richard Lewontin's book The Triple Helix
This field of research is called eco-evo-devo, which is short for Ecological Evolutionary Developmental Biology. It builds on the groundbreaking discovery of a highly conserved 'genetic tool kit’ that regulates the development of all animals. Over the last four decades, evolutionary developmental biology (evo-devo) has revealed that this “genetic toolkit” sets up the body plan of all animals. For example, the development of eyes, as different as the compound eyes of flies and complex camera eyes of vertebrates, is regulated by the same toolkit gene called eyeless/Pax-6. The ectopic expression of the mouse Pax-6 gene within the developing wing of a fly can induce the development of an eye on its wing. These findings naturally lead to the following fundamental question––if all animals have similar genes in their genetic toolkit, like eyeless/Pax-6, how is it that animals have evolved to be so diverse in form? eco-evo-devo, with its integrative approach, holds the promise to providing key insights into this question.
General overview of eco-evo-devo from the Abouheif lab:
Abouheif E, Favé MJ, Ibarrarán-Viniegra AS, Lesoway M, Rafiqi AM, and Rajakumar R. 2014. Eco-Evo-Devo: the time has come. Pgs 107-125 in C.R. Landry and N. Aubin-Horth (eds.), Ecological Genomics: Ecology and the Evolution of Genes and Genomes, Advances in Experimental Medicine and Biology 781. doi.org/10.1007/978-94-007-7347-9_6. Springer
We see nature through the ant, and the ant through eco-evo-devo
A soldier from the ant genus Pheidole. Image from Ant Web
We primarily focus on ant societies as a model for our eco-evo-devo studies. The division of labor in ant societies, which rivals human societies in its complexity, has made ants one of the most ecologically diverse and evolutionarily successful organisms on our planet, with the ~15000 species making up more than half of the global insect biomass.
A key trait that has enhanced the division of labor in ants is the evolution of morphological castes, like the winged queen and her wingless workers. The differences between queens and workers can be dramatic – queens possess fully functional wings, are reproductively active, and can live up to 30 years, while workers are wingless, reproduce rarely, and live for just a few months. These dramatic differences between castes are called “polyphenic,” which means they develop largely as a consequence of environmentally induced differences in gene expression during queen and worker development.
Queen and worker of the ant genus Lasius. Image from Alex Wild
An ant colony can be thought of as a 'superorganism', where the reproductive queen is like the 'germline' of the colony and non-reproductive workers is like the 'soma' of the colony. In essence, these morphological castes in a single ant colony are analagous to the different cell types within a multicellular organism. Therefore, by understanding how morphological castes differentiate and evolve to form complex ant colonies, we can learn about the processes through which different cell types within a multicellular organism differentiate and evolve to form complex multlicellular organisms.
A major goal in the Abouheif lab is to uncover how novel castes originated during the origin and evolution of ant societies. Here are three general research themes in the lab:
Uncovering the eco-evo-devo mechanisms underlying the origin and evolution of wing polyphenism in ants
Left or Top: Queen and Worker from the genus Stigmatomma. Right or Bottom: The high conserved wing patterning network. Ant Image Alex Wild
Eusociality and wing polyphenism in ants originated together approximately 150 million years ago. In contrast to the later evolved ant lineages, where the morphological differences between castes are striking, societies in the basal lineages are comprised of queen and worker castes that are morphologically similar and can both mate and reproduce. The only major morphological difference between castes is the presence of wings on queens and their absence on workers, which is thought to be the key genetic step that prevented workers from dispersing from their colonies. We are searching for the eco-evo-devo mechanisms that may have led to the origin of wing polyphenism in ants. Publications related to Theme 1:
Behagues J, Fisher BL, Péronnet R, Rajakumar R, Abouheif E and Molet M. 2018. Lack of interruption of the gene network underlying wing polyphenism in an early-branching ant genus. JEZ-B: Molecular and Developmental Evolution: 1-9. doi.org/10.1002/jez.b.22794
Uncover the eco-evo-devo mechanisms underlying the origin and evolution of the reproductive division
of labour in ants
Oocyte from the ant genus Lasius. Image by A. Khila
The reproductive division of labour between queens and workers is the hallmark of eusociality. A main interest in the Abouheif lab is to understand the molecular and developmental mechanisms that produce a queen with fully functional ovaries that can lay millions of eggs in her lifetime or a worker with either reduced reproductive capacities or are completely sterile. This is key for understanding ant colonies as superorganisms develop and evolved a germline / soma division. Publications related to Theme 2:
Khila A and Abouheif E. 2008. Reproductive constraint is a developmental mechanism that maintains social harmony in ants. Proceedings of the National Academy of Sciences, USA 105:17884-17889, doi.org/10.1073/pnas.0807351105
Khila A and Abouheif E. 2010. Evaluating the role of reproductive constraints in ant social evolution. Philosophical Transactions of the Royal Society of London Series B 365: 617-630, doi.org/10.1098/rstb.2009.0257
Uncover the eco-evo-devo mechanisms underlying origin and evolution of complex worker caste
systems in ants
Workers in a single colony of carpenter ants (top), big-headed ants (left), and Colobopsis ants (right).
During ant evolution, the worker caste diversified into a complex system of worker subcastes, like that found in the ant genus Pheidole. A discovery lead by the Abouheif lab (Rajakumar et al. 2012, Science) showed that ancestral genes, which lay dormant for millions of years, can be revived with the right environmental triggers. Three kinds of workers – minor workers, soldiers and supersoldiers – can be observed in the ant genus Pheidole. Although all Pheidole species have minor workers and soldiers, the supersoldiers were lost early in the evolution of the genus about 35 to 65 million years ago and are absent from almost all Pheidole species. We showed that Pheidole species that lack supersoldiers still retained an ancestral developmental potential to produce supersoldiers – it was possible to trigger the release of this hidden supersoldier potential by applying high doses of hormone at a critical stage in the larvae’s development. These dormant potentials exist in all animals, as reflected by the sporadic appearance of ancestral traits in individuals that normally should not have them. These traits, such as bird’s teeth and snake’s fingers, are widespread in nature but are traditionally thought to be “freaks” that contribute little to the evolutionary process. Our discovery in Pheidole supersoldier ants shows that these dormant genetic potentials, once triggered, act as raw materials for evolution changing this traditional view.
What stores this ancestral developmental potential for 35-60 million years in Pheidole ants and what facilitated the evolution of a novel supersoldier subcaste? We recently discovered (Rajakumar et al. 2018, Nature) that wing rudiments, which transiently appear during development)of the wingless worker castes, store these dormant potentials in ants for millions of years and generate novel worker subcastes in ants.
Together, these three research themes will take us a step closer to understanding the origins and diversification of a complex biological system.
The Abouheif Lab would like to graciously thank the following funding agencies for providing financial support for this research: