The genomic origin of species: a comparative study in the Australian Meliphagoidea

A project undertaken at CSIRO National Research Collections Australia and supervised by Leo Joseph

Unraveling the mechanisms underlying the process of speciation has been pursuit of evolutionary biologists since Darwin. The rich continental-scale Australian vertebrate biodiversity provides a powerful framework to take a comparative approach in studying this process. Although it takes millions of years for speciation to complete, many pairs of populations are currently exists at different stages of this trajectory: incipient species. This provides the perfect setting to study how incompatibilities accumulate between populations through time to the point where they may be considered full species. Understanding the process of speciation provides insight on how different factors influence species formation and, ultimately, how biodiversity has, and will be, formed.

Conveniently, the speciation process can leave footprints throughout the genome. By observing the movement of genomic regions between incipient species pairs at different stages of speciation, we will understand the accumulation of barriers to gene flow. The project will focus 13 incipient species pairs within the avian group meliphagoidea; comprising of fairywrens, honeyeaters, pardalotes, etc. The focal pairs have a shared zone of contact in northern Queensland, dividing the Cape York and central Queensland populations. To compliment the genomic data, morphology and plumage data will be collected to understand the interplay between genomic and phenotypic differentiation. Taking an intrinsic (genomic) and extrinsic (phenotypic) perspective provides an integrative approach to studying the process of speciation in an iconic Australian avian group.

Scientific Objectives
  1. Test the prediction that genome-scale introgression is inversely proportional to population divergence. Hybrid zones between incipient species at different stages of differentiation provide a natural experiment of the breakdown of isolating barriers between diverging populations.
  2. Test the prediction that divergent regions in the genome (“islands of divergence”) expand to neighboring regions (“continents of divergence”) in species-pairs further along the speciation process.
  3. Test the prediction that phenotypic divergence serves as a proxy for gene flow. With similar genomic divergence, we would predict that gene flow would be more restricted between populations exhibiting phenotypic divergence compared to phenotypically homogenous populations. By comparing the distribution of genomic and phenotypic introgression through space and time we would shed light on how extrinsic selective pressures (ecological and social) that act on the phenotype and intrinsic selective pressure acting on the genome all influence gene flow.
  4. Shed light on the role that hybridization may play in speciation. The degree to which hybridisation may speed or slow speciation is a debated topic, which would greatly benefit from a large comparative study as proposed here.

Initial results have shown wide variation in genetic divergence and genetic exchange between bird populations from the Cape York Peninsula and central Queensland. This region in Australia is an example where many populations at various stages of speciation co-occur. Sampling throughout the region has also showed that genetic exchange between some populations are localized while others are geographically broad and rampant. This sets up further questions regarding the interplay between the external environment and intrinsic genetic incompatibilities and how it influences variation in gene exchange throughout the genome.  Also, by developing a high quality genome of the Superb Fairy-wren, we have a genomic resource to apply to all Meliphagoidea and so understand the genetic shifts in speciation right down to the level of which genes are most affected.

Publications

Peñalba, J. V., Mason, I. J., Schodde, R., Moritz, C., & Joseph, L. Characterizing divergence through three adjacent Australian avian transition zones. Journal of Biogeography. 2017;00:1–12. https://doi.org/10.1111/jbi.13048

Figure 1. Yellow-spotted Honeyeater Meliphaga notata, one of the so-called “mimic’ honeyeaters, which comprises a group of very confusingly similar-looking species but which differ in habitat, vocalizations and size.

Figure 2. Tropical Scrubwren Sericornis beccarii. The relationships between this and he Large-billed Scrubwren S. magnirostra have been a challenging question for some time and the project is examining the details of their history of speciation.