My overall research goal is to understand the connections between macroevolutionary patterns of diversity, and population-level processes (e.g., natural selection).  At a broad scale, I am primarily interested in two complementary questions:               

How do ecological and population genomic forces interact to shape adaptive evolution and organismal diversity? 

How do major transitions in life history influence how organisms interact with their environment?

I address these questions primarily through the study of plants and herbivorous insects (including some specialised herbivores occasionally referred to as pollinators).  My work bridges four primary levels of inquiry: Comparative (phylogenetic) analyses; Field studies in natural habitats; Phenotypic analyses (e.g., chemical ecology); Genomics.  

Currently, I am a P3 Independent Research Fellow at Sheffield University.  I completed my PhD at Cornell University with André Kessler and was then an independent Banting Fellow at the University of Toronto with Spencer Barrett and Stephen Wright.  Major themes in my current research are described below.

[1] (Co)evolution of REPRODUCTION, functional traits and species interactions.

The extraordinary diversity of plants and insects has long been attributed to coevolutionary interactions. For example, the interactions of pollination and herbivory have likely given rise to two seemingly unrelated components of plant diversity: reproduction, exemplified by the stunning diversity in flower form and function; and defence, exemplified by the remarkable variation in volatile and non-volatile secondary metabolites. Long studied as separate processes, my research has focussed on interactions between reproduction/pollination and defence/herbivory as an important source of biodiversity.

I have been examining how the evolutionary loss of self-incompatibility (i.e., enforced outcrossing) has shaped the evolution of defence and the diversity of plant secondary metabolites.  Much of my work has focused on self-incompatible and self-compatible species from across the Solanaceae, from petunias to potatoes, using a combination of experimental and phylogenetic approaches. The results of these comparative studies (e.g., Campbell & Kessler 2013) have suggested that defence strategies and reproductive strategies in plants are coevolving. They have also indicated that the evolution of floral and leaf chemistry, and natural selection by both herbivores and pollinators, are modulated by the plant's mating system.  I am seeking to disentangle these interactions (mating system-pollination-herbivory) across numerous wild species within the Solanaceae (particularly wild tomatoes and potatoes) and Brassicaceae (see below).  Since pollinator-herbivore interactions involve complex, volatile-mediated floral signalling, some of this work focuses on understanding the poorly understood effects of mating systems and herbivory on floral volatile evolution.  Read more... 

[2] Evolutionary genomics of defence and reproduction.

Transitions from outcrossing to selfing alter many important evolutionary and ecological processes, including genetic diversity, the genome-wide strength of natural selection, demography, and the ability to colonise marginal, novel environments. In other words, adaptive evolution in selfers should result from the interplay of population genetic effects predicted by theory, and directional selection by the biotic and abiotic environment. However, the interaction of ecological selection and the genome-wide effects of mating system variation remains poorly understood.  As part of my research as a Banting Fellow at the University of Toronto, I have been using comparative and population genomics coupled with field experiments to examine the evolution of defence, floral traits and mating systems. This work focuses on the repeated evolution of selfing in the predominantly outcrossing wild mustard, Arabidopsis lyrata (Brassicaceae), from northern Ontario to North Carolina.

[3] INBREEDING DEPRESSION UNDER STRESS. 

Sexual reproduction is highly variable, and yet we are only beginning to understand how this variation influences interactions with predators and parasites and how these enemies, in turn, impose natural selection on mating systems.

Plants which can self-fertilise have a range of mating options available to them: they can self-pollinate, they can exchange pollen with relatives, and they can outcross to a non-relative. Each of these “choices” (as determined by population size, plant condition, pollinator availability, stigma receptivity, incompatibility system, etc) will carry different consequences for the offspring.  For example, the progeny of inbreeding (the first two cases) may experience inbreeding depression, as a result of more of their loci being homozygous (which in turn exposes any deleterious recessive mutations). The exposure of mildly deleterious alleles can occur at any locus, but of particular interest are those loci which are linked to fitness, including ecological traits such as plant defences. Using self-fertilised and outcrossed families of the wild Solanaceous plant Solanum carolinense L. (horsenettle, pictured at left with some native herbivores), I have found that reductions in defensive secondary metabolites due to inbreeding lead to significant herbivore-mediated ecological inbreeding depression in nature.  This research used replicated herbivore exclusion on multiple genetic families in the field to unambiguously demonstrate the potentially strong role of herbivores as agents of natural selection on mating systems. Horsenettle is mostly outcrossing and is expected to exhibit strong inbreeding depression - excellent multi-population work in other systems (e.g., Carr, Eubanks and colleagues; Leimu and colleagues; Nuñez-Farfán and colleagues, among others) suggests that this process may be complicated in species that inbreed more readily than horsenettle. Inbreeding also affects herbivore-induced, phenotypic plasticity in both resistance and tolerance traits.  The deleterious effects of inbreeding on plasticity (i.e., inducibility) appear to be mediated by reductions in the production of key phytohormones.  Thus, intraspecific plant mating system variation influences chemically mediated ecological interactions, and these interactions in turn can influence the maintenance of outcrossing. Read more...