SPECIATION AND ADAPTATION TO NOVEL ENVIRONMENTS
The process of speciation, despite its overwhelming role in the origins of biodiversity, remains poorly understood. For sexually reproducing organisms defined by the Biological Species Concept, we still are unclear regarding many basic questions: How often does sympatric rather than allopatric speciation occur? What are the relative roles of sexual behavior, postcopulatory-prezygotic incompatibilities, and postzygotic problems such as hybrid sterility and inviability in reproductive isolation? Is there a particular degree of genetic differentiation associated with the appearance of one or more of the categories of isolating mechanisms? What is the role of ecological adaptations in reproductive isolation?
In order to address these issues in a comprehensive framework, we need to utilize a group of organisms that not only is ecologically defined, but one for which we can employ modern molecular approaches. One group of organisms, the cactus breeding Drosophila (fruit flies) of the Sonoran Desert of North America, are ideally suited to studies of adaptation and speciation. Four species of Drosophila are endemic to the Sonoran Desert of North America: D. nigrospiracula, D. mojavensis, D. mettleri, and D. pachea. Each uses the necrotic tissue of a different columnar cactus species as a feeding and breeding site, with the exception of D. mettleri, which breeds in soil beneath a necrotic cactus that has been soaked with necrotic juice.
The Sea of Cortez separates the portion of the Sonoran Desert found in Baja California from the part on Mexico's mainland, acting as a barrier to gene flow for many organisms. We utilize molecular markers (Ross et al. 2003; Hurtado et al. 2004) to study the degree to which populations of different Drosophila species from the two sides of the Sea of Cortez exhibit differentiation with respect to genetics. We then measure reproductive isolation at the pre- and post zygotic levels (Reed & Markow 2004), especially assortative fertilization (Markow 1997) to test hypotheses regarding when reproductive isolation appears, and in what form, relative to the earliest stages of genetic differentiation.
Cacti have a very different chemical composition compared to the host resources used by most Drosophila species. They are very low in nitrogen and phosphorus (Markow et al. 1999; Jaenike & Markow 2003) and they contain chemicals that are toxic to many species of organisms. Yet the resident Drosophila species can feed and breed in these plants without ill effects. We employ functional genomic approaches, custom microarrays for D. melanogaster and D. mojavensis, to study the genes involved in the utilization of different dietary resources by Drosophila melanogaster (Cartsen et al. 2005) and Drosophila mojavensis (Matzkin et al. 2005). We also study the influence of nutrients on growth rates in Drosophila species that specialize on nutrient-rich versus nutrient-poor food (Watts et al. 2005)
MATING SYSTEM EVOLUTION
Species of the genus Drosophila exhibit amazing variability in mating system characters such as age at reproductive maturity, sexual dimorphism in age at reproductive maturity, sperm length, ovariole number, female incorporation of ejaculatory substances, copulation duration, and the presence or absence of male secondary sexual characters (Markow 1996; Markow 2002; Markow and O'Grady 2005). The laboratory is interested in identifying the long-term evolutionary as well as the ecological (Markow et al 2001) factors that underlie this variation. See Powerpoint of sperm length figure for here. Mechanisms of postcopulatory but prezygotic reproductive isolating mechanisms are likely to be rooted in mating system evolution. Interactions between male and female reproductive molecules and morphology are potentially involved in incompatibilities that occur after mating but before fertilization. Reproductive isolating mechanisms that operate at this level could be due to mismatches between either the morphological (Pitnick et al 2003) or the molecular characteristics (Knowles and Markow 2001) of male and female reproductive tissues.
DROSOPHILA EVOLUTIONARY GENOMICS
The NSF-supported Stock Center is a living collection of more than 1600 strains of over 250 species of Drosophila. The genomes of 12 of these species are now fully sequenced. Sequenced species vary widely with respect to traits like morphology, longevity, learning ability, and resistance to stressors like chemicals, heat, desiccation, starvation that make them ideal model systems for biomedical studies.
Bono, J. M., Matzkin, L. M., Kelleher, E. S., Markow, T. A. 2011. Postmating transcriptional changes in reproductive tracts of con- and heterospecifically-mated Drosophila mojavensis females. Proceedings of the National Academy of Sciences, in press.
Matzkin, L.M., Johnson, S., Paight, C., Bozinovic, G., and Markow, T.A. 2011. Dietary protein and sugar differentially affect development and metabolic pools in ecologically diverse Drosophila. Journal of Nutrition, in press.
Hardy, R., Lougheed, A. and Markow, T.A. 2011. Reproductive tract and spermatid abnormalities of hybrid males from reciprocal crosses betweenDrosophila mojavensis and D. arizonae. Fly, in press.
Song, X., Goicoechea, J.L., Ammiraju, S.J.J., et al, (Markow, T.A., corresponding author). 2011. The 19 genomes of Drosophila: a BAC library resource for genus-wide and genome scale comparative evolutionary research. Genetics, in press.
Kelleher, E.S., Clark, N. and Markow, T.A. 2011. Diversifying selection acts on a female reproductive protease family in four subspecies of Drosophila mojavensis. Genetics, doi: 10.1534/genetics.110.124743.
Markow, T.A. and Pfeiler, E. 2010. Mitochondrial DNA evidence for deep genetic divergences in allopatric populations of the rocky intertidal isopod Ligia occidentalis from the eastern Pacific. Molecular Phylogenetics and Evolution 56:468-473.
Kelleher, E.S., Watts, T.D. LaFlamme, B., Haynes, P. and Markow, T.A. 2009. Proteomic Analysis of Drosophila mojavensis Male Accessory Glands Suggests Novel Classes of Seminal Fluid Proteins. Insect Biochemistry and Molecular Biology 39:366-371.
Kelleher, E.S. and Markow, T.A 2009. Duplication, selection, and gene conversion in a Drosophila mojavensis female reproductive protein family. Genetics 181:1451-1465.
Dr. Markow is a new faculty member at U.C. San Diego.