arthropod evo devo

I use arthropod appendages to understand how animal bodies (and the gene networks that build them) evolve over huge timescales of hundred of millions of years.

My research area is evolutionary developmental biology (evo devo), and I use mainly the crustacean Parhyale, the beetle Tribolium, and the millipede Oxidus, but also sometimes horseshoe crab, tarantula, silverfish, sea spider, and other arthropods. My lab uses molecular, morphological, and embryological approaches to investigate arthropod appendages like legs, wings, and gills as a model to understand the origin of novel structures that have never existed before, and to elucidate how gene networks evolve over immense phylogenetic distances of half a billion years.

Ultimately, I am interested in how gene networks change to produce different kinds of animal bodies (morphological diversity). For example, it has been repeatedly observed that structures which look and function very differently -- like legs and genitalia, or insect wings and crustacean gills -- can nevertheless share the same gene network. The most common explanation for this has been that one structure co-opted the gene network of the other structure, meaning that the structures themselves are unrelated (not homologous) even though their gene networks are related (homologous). This model has been called “deep homology”.  But instead of recent gene network co-options, my research has led me to ask, What if these very different structures that share the same gene network really did evolve from the same structure in their shared ancestor,  but the structures have just been modified beyond our ability to recognize their relationship? 

These two different models provide contrasting explanations for the origin of novel structures – such as insect wings and insect tracheae. Novel structures are often defined as structures that are not derived from (homologous to) any structure in the ancestor nor any other structure in the same organism. Co-option of gene networks into unrelated (non-homologous) contexts has been invoked for decades to explain the origin of novel structures, but recently, my research into novel structures in arthropods has suggested an exciting alternative: ancestral structures can persist in a cryptic, unrecognizable form in intermediate lineages and then become elaborated again in later lineages, which makes the ancient structure appear as if it is novel. I have termed this model for the origin of novel structures “ancient homology” to reflect the relatedness (homology) of both the structures and their gene networks, in contrast to “deep homology” which posits homology of gene networks but not the structures themselves. 

Beyond novel structures, my ancient homology model appears to be a fruitful framework for understanding the general evolution of morphology and gene networks over huge timescales on the order of half a billion years. 

The system in which I explore ancient homology is the ectodermal outgrowths of arthropods. There are four major groups of arthropods: chelicerates (spiders, etc), myriapods (millipede, etc), crustaceans (non-insect crustaceans like shrimps, etc), and insects (beetles, etc). Arthropods have been diverging from each other for half a billion years, accumulating an incredible diversity of ectodermal outgrowths like wings, carapaces, gills, helmets, horns, and abdominal teeth, many of which have been called novel structures. Researchers have been arguing about these and other arthropod outgrowths for nearly two centuries, amassing a rich body of literature to mine on their morphology, embryonic development, and, more recently, molecular patterning. At the center of these arguments is the origins and relationships of these outgrowths: did each structure evolve de novo in each lineage, or could they be related somehow? 

In my Ph.D and postdoc, discovered a simple molecular method for deciphering the origins and relationships of all arthropod ectodermal structures, which surprisingly revealed that most of these so-called novel structures are in fact anciently related (as serial homologs).  This simple method thus unlocks arthropod ectodermal outgrowths as a powerful system in which to elucidate how evolution changes gene networks to generate all the spectacular diversity of animal bodies that have evolved over hundreds of millions of years.

To build models of how morphology—and the gene networks that create it—evolves over immense timescales of half a billion years, research at the Ancient Homology Lab investigates the near-endless plethora of arthropod outgrowths. We use morphological, embryonic, and molecular methods to compare structures between three arthropod species that have been diverging from each other for half a billion years: the flour beetle insect, Tribolium castaneum, an established model insect; the genetically tractable amphipod crustacean Parhyale hawaiensis; and the millipede Oxidus gracilis.  

My work has deep implications for understanding the evolution of animal bodies (morphology) and gene networks. For example, it is often assumed that when structures that look and function very differently yet share the same gene network – such as legs and genitalia, or insect trachea and hormone glands – it is because one structure “co-opted” the gene network of the other. But my work instead suggests that these very different structures may have actually descended from the same structure in their very ancient (e.g. pre-Cambrian) ancestor, and simply been modified beyond all recognition. This means that 

1. The persistence of cryptic, unrecognized ancient structures in a lineage may offer a better explanation than gene network co-option for why gene network-sharing is so commonplace. 

2. Cryptic persistence means that many structures, even those that seem new, may actually have incredibly ancient origins.

3. This is related to the hourglass model of development: when very ancient structures duplicate and diverge, the identity-conferring part of the gene network (Hox genes, heart genes, leg genes, etc) would remain largely intact, but the downstream part of the gene network that creates a structure's shape, size, and function (morphogenesis and differentiation genes) will have undergone extensive systems drift to generate very different-looking structures, like legs and genitalia, or insect trachea and hormone glands). This process would result in structures so highly modified that it appears as though two unrelated structures share the same identity-conferring gene network.

4. Repeated structures in an individual (serial homologs) – such as placode-derived teeth, hair, sweat glands, and mammary glands in mammals – can be organized into a phylogenetic tree according to when each structure began diverging in function. The phylogenetic and developmental relatedness between two structures in an individual is likely to predict how readily their gene networks can be swapped. For example, the relatedness of genitals and legs as serial homologs likely explains the ability of the genitalia in Drosophila to activate the leg-derived spiracle-forming gene network to generate a new structure on the male genitalia, the posterior lobe. In this way, the evolution of “novel” structures is likely to have a degree of predictability.

     Insects (beetles, etc)                       Crustaceans (shrimp, etc)

     Myriapods (millipedes, etc)           Chelicerates (spiders, etc)

I am interested in working on any arthropod ectodermal outgrowths ("stick-outty thing") in any arthropod or near-arthropod! Let's figure out what that stick-outty thing is :) 

My Department of Zoology profile at University of British Columbia:

https://zoology.ubc.ca/person/heather-bruce