Rapid evolution

in Drosophila melanogaster 

across seasonal time

RESEARCH

The rate and tempo of evolutionary processes is fundamental across different time scales ranging from local adaptation to speciation. My research interest focuses on understanding the genetic basis complex traits and behaviors that evolve rapidly within and between species. I address these questions in natural populations of the genus Drosophila to use the tools and resources from the genetic model D. melanogaster. My dissertation research focused on intraspecies evolution rate and genetic architecture of rapid adaptation across very short seasonal timescales. As a postdoctoral fellow, I examine evolution across longer evolutionary periods to understand the genetic and neuronal mechanisms of behaviors that evolve rapidly between species.

Timescale

local adaptation within

a species

evolution

 between

closely related species

short

Long

Timescale

Annual seasonal rhythms produce rapid, predictable environmental changes that may produce rapid, cyclic adaptation in multivoltine species that reproduce multiple times each year. Drosophila melanogaster is a powerful system to evaluate the genetic architecture of rapid evolution in response to predictable environmental changes produced by annual seasonal rhythms. D. melanogaster populations in temperate North America persist in orchards across changing seasonal climates and variations in food type and abundance. The strenuous selection imposed by fluctuating environmental conditions creates a grand naturalistic experiment. I sampled D. melanogaster populations at different time points and measured traits in a common garden laboratory environment.

Behavioral evolution

of prezygotic reproductive isolation between closely related species

I find that suites of complex fitness traits change incredibly rapidly in a predictable way over the 10-15 generations from spring to fall and return back during the 1-2 generations that occur overwinter between fall and spring. The harsh winter selects for a suite of traits that produce a robust spring population characterized by an increased investment in somatic maintenance: higher resistance to thermal stress, higher tolerance to pathogenic infection, faster development time and better learning. Those traits decline throughout the summer when ripe fruit is abundant due to correlated trade-offs with reproduction; this results in a fall population that is less stress resistant but highly fecund. The seasonal trade-off between winter selection for stress resistance and summer selection for reproduction encapsulates the classic life history trade-off between reproduction and somatic maintenance.

Whole genome resquencing of the populations identify hundreds of alleles that cycle in frequency across seasonal time; the oscillations in allele frequency change repeat across years and are not due to migration. I assess the function of the alleles that cycle in frequency across seasons using complementary forward and reverse genetic approaches. Seasonal alleles are in pleiotropic genes with functional effects on multiple traits and non-additive epistatic interactions in genes that effect these traits are prevalent and shape the genetic architecture of change across seasonal time.

In summary, there is rapid, repeatable adaptation to abiotic and biotic environmental parameters that cycle as a function of seasonal time. Pleiotropy and epistatic interactions within and among genes are pervasive and facilitate the rapid evolutionary changes that occurs over timescales previously considered static.

As species diverge, reproductive isolation can be reinforced through behavioral differences that signify species identity and discourage interspecies courtship. Courtship rituals evolve rapidly and serve as a strong prezygotic reproductive barrier between closely related species. Drosophila courtship displays consist of a series of discrete behaviors with species-specific modifications. Components of courtship within the Drosophila melanogaster subgroup have rapidly diversified. I am using comparative approaches to understand the genetic basis of how homologous neural circuits evolve to produce divergent behaviors. My research focuses on two components of the courtship ritual: tapping and singing.

Males taste species- and sex-specific pheromones by tapping potential mates with their front leg. Tapping serves as a tipping point that encourages conspecific mating by initiating courtship behaviors and suppresses courting an inappropriate mate. I am studying the genetics of how

the same pheromone stimulus travels through a homologous neural circuit to produce opposite behaviors.

 

If the male proceeds to court, one of the behaviors in his repertoire is vibrating his wings to sing  to the female. Courtship song evolves rapidly, presumably as a result of female-choice sexual selection, and each species sings a unique variation of the repertoire of signals with differences in carrier frequency and inter-pulse interval (IPI). I am interested in the genetic basis of how the components of song evolve among closely related species.