Research

We are Eco-Evo-Devo...


We are in the midst of a conceptual revolution in the biological sciences as the traditional borders between ecology, molecular, 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, and how this interaction generates novelty in complex biological systems.

This field of research is called Eco-Evo-Devo, which is short for Ecological Evolutionary Developmental Biology. It builds on the groundbreaking discovery that there is a highly conserved genetic ‘tool kit’ that controls the development of all animals. This tool kit is made up of a relatively small number of regulatory genes, such as the Hox genes (see Figure 1 below), which play a critical role in setting up segments along the anterior–posterior axis of all animals during development. Hox genes are clustered together in the genome and are expressed in the same order as their physical location on the chromosome. So, for example, the Hox gene labial (red boxes in Figure 1 below) occupies the first position in the cluster and is expressed at the head end of animals, while the Hox gene abdB is located at the end of the cluster and is expressed at the very tail end of all animals (blue boxes in Figure 1 below). The conservation of physical location, expression, and function of Hox genes in all animals is one of the great discoveries of biology, and has kept me fascinated for the last 20 years


Figure 1: Image from Billie J. Swalla " Building divergent body plans with similar genetic pathways"

So if all of these animals have similar genes in their genetic toolkit, like the Hox genes, how is it that animals have evolved to be so diverse in form? How novel features have evolved in complex biological systems to make animals so diverse in form is a central question in evolutionary biology that has remained unresolved for over 100 years. Eco-Evo-Devo, with its integrative approach, holds the promise to resolving this question, and as a consequence, will have many important benefits, like understanding how complex systems at all biological scales originate and diversify or making evolutionary theory more predictive, and of course, more practical benefits, like improving animal/plant breeding, biodiversity conservation, and medicine.

We see nature through the ant, and the ant through Eco-Evo-Devo


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 novel morphological castes, like the winged queen and her wingless workers (see Figure 2).


Figure 2: Queen and Worker of the ant genus Lasius. Image from Alex Wild

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.

A major goal in the Abouheif lab is to uncover how novel worker castes originated during three major 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)
  2. The “point of no return” (when eusociality becomes irreversible because the reproductive capacity of workers is significantly reduced)
  3. The diversification of a single worker caste into a complex system of morphological and behavioral subcastes.

 

Project 1
Uncover the developmental genetic mechanisms during or after the first major transition:
the origin of eusociality

 

Figure 3: Wingless worker of the basal ant species Harpagnathos saltator. Image from Alex Wild

The first major transition during ant evolution – the origin of eusociality – occurred ~150 million years ago and is associated with the origin of a novel wingless worker caste (see Figure 3). In contrast to the later evolved ant lineages, where the morphological differences between castes are striking, societies in the ancestral lineages are comprised of queen and worker castes that are morphologically similar and can both mate and reproduce (compare Figure 4 to Figure 1). 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 (see Figure 4).


Figure 4: Queen (center) and worker (top) from a basal species of ants (left side) and gene network regulating wing development (right side). Image of ants from Alex Wild

We are searching search for the developmental and genetic mechanisms that may have led to the loss of wings in the worker caste.

Project 2
Uncover the developmental and genetic mechanisms during or after a second major transition:
the Point of No Return


Figure 5: Queen and workers from the ant genus Monomoium. Image from Alex Wild

The second major transition during ant evolution – the point of no return – is thought to indicate the point at which eusociality becomes irreversible through the evolution of worker castes that are morphologically distinct and show reduced reproductive capacity relative to the queen caste (see Figure 5). Papers from the Abouheif lab (Khila and Abouheif 2008 and 2010) suggest that we are on the verge of discovering a novel developmental mechanism underlying this reduced capacity to reproduce in workers (see Figure 6).


Figure 6: The oocyte of an ant queen showing alpha-tubulin in green, actin in red, and nuclei in blue. Image from Khila and Abouheif 2010.

 

Project 3
Uncover the developmental and genetic mechanisms during the third major transition:
a complex system of morphological and behavioral subcastes

 


Figure 7: Minor worker (smallest size), soldier (medium sized) and supersoldier (supersized) ants from the genus Pheidole. Image from Alex Wild

The third major transition in ant evolution is marked by the diversification of a single worker caste into a complex system of worker subcastes, like that found in the ant genus Pheidole (Figure 7). A recent discovery in 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. Though supersoldiers were lost in this genus about 35 to 65 million years ago, we showed it was possible to unlock this hidden genetic potential by applying high doses of hormone at a critical stage in the larvae’s development. Wing precursors called "wing imaginal discs" as well as the gene network regulating wing development (Figures 4 & 8) are key to understanding these dormant genetic potentials in ants.

Figure 8: A wing imaginal disc of a queen showing the expression of the spalt gene (see sal in gene network regulating wing development in Figure 3 left).

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 shows that these dormant genetic potentials, once triggered, act as raw materials for evolution changing this traditional view. Our next step is to uncover the developmental and genetic mechanisms driving the evolution of novel worker subcastes in ants.

Together, these three projects will take us a step closer to understanding the origins and diversification of a complex biological system.

----------------------------------------------------------------------------------------------------------------------------------------

Funding Agencies

The Abouheif Lab would like to graciously thank the following funding agencies for providing financial support for this research:

Natural Sciences and Engineering Research Council
NSERC home: http://www.nserc.ca/index.htm

McGill University, http://www.mcgill.ca

Fonds de recherche sur la nature et les technologies
FQRNT home: http://www.fqrnt.gouv.qc.ca/




Canadian Foundation for Innovation
CFI home: http://www.innovation.ca/

Canada Research Chairs
CRC home: http://www.chairs.gc.ca/web/home_e.asp

National Science Foundation
NSF home: http://www.nsf.gov/

Alfred P. Sloan Foundation
Sloan Foundation home: http://www.sloan.org/


Scientific Societies and Journals supporting EvoDevo