MATE CHOICE AND THE BIOENERGETICS OF BEHAVIOUR
My research is shaped by my background in behavioural research, specifically in the sexually selected displays of birds. To reach a fundamental understanding of such emergent characteristics of complex animals, many of my studies are of the mechanisms that underlie the production of traits--including, most recently, mitochondrial bioenergetics. By better understanding the genetic and physiological underpinnings of such displays, we can better explain the role of such displays in maintaining species boundaries and, ultimately, shaping speciation processes themselves.
CAROTENOID-BASED COLOURATION IN BIRDS
My Ph.D. research focused on testing the best-accepted hypothesis for why the expression of particular coloured ornaments in birds (those formed by carotenoid pigments) often correlates with aspects of physiological quality. The “resource trade-off hypothesis” proposes that individuals face a costly trade-off between retaining carotenoid pigments for internal benefit (they have antioxidant properties) versus “spending” them as ornamental colourants (see this review). To test this hypothesis, I examined measurements of oxidative and immune health in a novel system with carotenoid knock-down mutations: white and yellow canaries. I found that carotenoid-deficient white canaries (left, bottom) performed indistinguishably from carotenoid-rich yellow canaries (left, top) on a suite of physiological measurements (results here), presenting a major empirical challenge to the longstanding hypothesis.
Such a dramatic null result demands explanation and further testing, so my current research explores new hypotheses that have the potential to link display trait expression to the quality of internal physiological processes without invoking resource trade-offs (see here and here). Mitochondrial presents a surprising, yet promising series of mechanistic explanations for variation in display behaviours. These mitochondrial function hypotheses have been well received but have not been definitively tested--yet. See the next section for how I am planning to test mitochondrial involvement in mate choice using the model fruit fly system.
Plasma isolated from whole blood in capillary tubes from yellow (top) and white (bottom). The colour indicates the presence and absence, respectively, of circulating carotenoid pigments.
DOES MITOCHONDRIAL PERFORMANCE SHAPE DISPLAY QUALITY?
Biomedical research has established clear mechanistic links between many processes related to sexually selected mating displays and mitochondrial function--both in cellular respiration and in signalling.
Sometimes, these relationships are indirect. For example, mitochondria lie at the hub of a multitude of signaling pathways for innate immune system development and function such that high-functioning mitochondria are necessary for effective immune defense. In turn, the expression of many mating displays has been found to correlate with measurements of immune system performance. Logically, then, displays that indicate immune system functionality may also indicate mitochondrial functionality.
Excitingly, some types of mating displays may have more direct connections to mitochondrial activity. The two we best understand to date are red carotenoid-based ornaments--see a recent study by my Ph.D. advisor's lab here--and cognitively complex displays, such as song (proposed here).
My current study system, the fruit fly, provides an outstanding opportunity to test this latter relationship in a controlled way not yet possible in vertebrate systems like songbirds. During courtship, male fruit flies "sing" by vibrating their wings in stereotyped rhythms that have been found to influence female mating decisions.
Working with the Monash Instrumentation Facility, I have built a 16-channel fruit fly song recording apparatus that allows me to detect and quantify the tiny fly song sounds, focusing on the speed of "pulses" (inter-pulse interval). I will use this apparatus to test how 1) varying mitochondrial genotype and 2) experimentally inducing mitochondrial dysfunction using targeted chemicals affects song performance.
A screen recording (top) of a snippet of fly courtship audio recording, playing on Audacity; the soft tapping sounds are examples of pulse song. Pairs of flies are set up to record in agar-filled vials stoppered with foam plugs (bottom).
Mate choice protoypes using LEGO bricks (top and bottom) show sets of chambers separated by a sliding central chain of bricks; the top photo depicts manually sliding the "door" open to introduce flies that have been in separate chambers. The bottom video shows the first protoype with clear demonstrations of male chasing and courtship--skip to 1:40 for the main action.
MITOCHONDRIAL VARIATION AND MATING SUCCESS
Variation in traits and signals is only important in an evolutionary sense if it influences variation in actual mating decisions. While song is a central component of courtship in both fruit flies and songbirds, successful pairing requires careful coordination of multimodal display components as well as effective behavioural tactics. I propose that many of these underlying mechanisms of mate attraction will be sensitive to mitochondrial functionality, but the overarching question is whether such variation may shape patterns of mate selection--and, consequently, gene flow within and across population boundaries.
My Ph.D. supervisor Geoff Hill specifically hypothesized that the need for high-functioning mitochondria drives the formation of species boundaries between populations that differ in their mitochondrial and mito-associated nuclear genotypes, yet this hypothesis remains difficult to test.
With a combination of in-depth ethological measurement and automated copulation success assays, I am testing whether mito-nuclear genotype affects mating decisions in my lines of fruit flies. I am currently developing the equipment needed for a high-throughput mating success assay--the prototype uses clear LEGO bricks. A sliding central set of bricks creates a sliding "door" that can simultaneously open a channel between separate chambers that have been pre-loaded with single males or females.
Further, in collaboration with an undergraduate student, I am working on a different protocol that assesses mating success when males are in competition with each other for a limited number of females. This procedure requires colouring males of different genotypes using bright pink or green powder (see left middle).