Are populations of marine invertebrates around the southern coast of Australia reproductively incompatible with each other?

A project undertaken at The School of Life & Environmental Sciences, Deakin University, Warrnambool and supervised by Dr Craig Styan

Many marine species have vast population sizes and widely dispersive larvae, both of which should ensure high gene flow and little genetic drift among local populations spread along a coastline. According to traditional population genetics theory, such large, well connected marine populations ought to make it very unlikely that reproductive barriers would ever develop among different parts of a species’ range - even among quite geographically-distant populations, because even trivial amounts of larval dispersal along a coastline should provide enough genetic mixing to prevent local populations from diverging genetically. I have, however, recently detected significant (genetically-based) gametic incompatibility between individuals from different locations within what appears to be one very widely distributed species of intertidal polychaete. The common intertidal tubeworm, Galeolaria caespitosa, is found in incredibly large numbers virtually everywhere on temperate Australian rocky coasts (see Fig. 1) and has larvae potentially capable of very widespread dispersal during 3 weeks of planktonic development. Yet, in cross-fertilisation assays, worms from Sydney and Adelaide were almost completely incompatible with each other in one cross-direction and even worms from Sydney and Ulladulla (just 220km along the coast) showed signs that eggs were less compatible with sperm from individuals not from their own population (Fig. 2).

One explanation for the partial reproductive incompatibility between worms in Adelaide and Sydney is that these populations represent separate, geographically separate (allopatric) species - which perhaps speciated when Bass Strait disappeared during recent glacial periods. Indeed, there is some molecular evidence that other widespread ‘species’ across eastern and southern Australia are actually unrecognized allopatric species complexes. Even still, the high level of incompatibility observed between these populations (species) of Galeolaria would still be unexpected between what must be only relatively recently separated groups - at least given the way we normally assume these processes develop, with reproductive divergence developing only slowly and secondarily as a by-product of geographic isolation of groups. Even more difficult for this model is the evidence of partial incompatibility between populations (Sydney & Ulladulla) which are very unlikely to have ever been isolated geographically. Instead, the answer here may be that reproductive incompatibility can develop independently within local populations despite some genetic mixing via larval dispersal and that this then leads to local populations becoming increasingly reproductively isolated from other local populations they still exchange larvae with.

This project will determine whether the type of reproductive incompatibility detected in Galeolaria is in fact widespread among other populations of G. caespitosa across its range and whether similar patterns of incompatibility also occur in other southern Australian marine species that have very different life history characteristics and geographic distributions. By using a series of cross-fertilisation assays and collecting independent (sequence-based) information about levels of genetic relatedness among geographically distant populations, patterns of incompatibility within and between populations of marine invertebrates on the pacific and southern coasts of Australia will be examined. In turn, this will enable models about the mechanisms which might have lead to reproductive barriers forming to be tested.

 
Figure 1. Large numbers of individuals of the common intertidal tubeworm, Galeolaria caespitosa. Each white tube houses an individual worm 1-3cm long.

Figure 2. Unfertilised egg (right) and three developing trochophore larvae (left). Using carefully designed fertilisation assays, incompatibility between sperm and eggs from different populations can be measured as a proportion of eggs not fertilising or developing in larvae.