Tim Vines

Stickleback Hybrid Zones

Hybrid zones form when two diverged populations come together and interbreed, creating a narrow band of hybrids. If these hybrids survive and breed themselves, their offspring will (on average) move slightly out of the contact zone, which widens the zone. However, hybrids may not be as fit as pure individuals, potentially because alleles from one parental species conflict with alleles from the other when they come together in a hybrid (=endogenous selection). In addition, if the hybrid zone has formed at an environmental transition, hybrids might be less fit because they are carrying the wrong alleles for their local environment (=exogenous selection). Low hybrid fitness prevents hybrids from moving very far from the zone, simply because most die or fail to reproduce before they get anywhere. Thus, for a given average dispersal distance, the width of the hybrid zone is controlled by the strength of selection against hybrids. That means we can estimate selection against hybrids (or genes) from the width of the zone.

We can estimate the average rate of dispersal into the centre of the zone from the associations between alleles at different loci (these associations are known as linkage disequilibria). A good analogy for linkage disequilibrium is mixing paint: imagine pouring red and white paint into opposite sides of a tray and stirring in the middle. If you stir only a little, most of the paint will be in red or white streaks, such that molecules of red paint will be closest to other red molecules (and vice versa for white). This is analogous to strong linkage disequilibrium, where alleles characteristic of the ‘red’ species at one locus are often found with ‘red’ alleles at other loci. If you stir a little more, pink paint will appear in the middle of the tray, and now red paint molecules are equally likely to be next to a white as to another red molecule. This is analogous to weak or zero linkage disequilibrium, where recombination has broken down the associations between ‘red’ or ‘white’ alleles at different loci. In fact, the classic model of hybrid zones (tension zones) are a dynamic equilibrium between pouring in paint, mixing, and mixed paint draining out a hole in middle of the tray (i.e. selection against hybrids). If the rate of inflow is high and the drain hole is large, most paint will be red or white, corresponding to a steep hybrid zone with strong selection and strong linkage disequilibrium. When the rate of mixing is high relative to the rate of inflow, and the drain hole is small, most paint will be pink and the ‘hybrid zone’ will be wide. We can therefore use amount of pink paint to infer (for a given zone width) to infer how quickly paint is coming in.

We now know a little about the types of genes that are involved in endogenous selection, mainly from studies of fruit fly species, but the genetics of exogenous selection are barely known at all. Fortunately, hybrid zones between stream and marine sticklebacks are absolutely perfect for investigating the effects of carrying the wrong alleles for your environment, because they often (but not always) occur at the transition between salt and fresh water, and there are many replicate zones all around the Northern hemisphere. More importantly, researchers in Stanford have identified a number of genes responsible for the phenotypic differences between marine and freshwater sticklebacks, and now that the stickleback genome is available, many more will come to light.

Stream-marine hybrid zones

Marine sticklebacks spend most of their lives at sea, and return to rivers and streams to breed. This makes them a bit like salmon, only smaller and less glamorous. We think that marine fish experience fairly intense predation from larger fish and birds in the sea, because they have long dorsal and pelvic spines and many (>30) bony armour plates along their sides. They are also relatively streamlined and well suited for feeding on plankton in open water. By contrast, stream resident fish live in freshwater all year round, have shorter spines and only a few armour plates. They also have a muscular hump behind their head, which increases jaw strength for rooting out prey on the stream bed.

Stream and marine sticklebacks meet when marines move into fresh water to breed, and in some watersheds they hybridise. After many generations of hybridisation, a stable hybrid zone can form, so that the population goes from pure marine fish through the entire range of intermediates to pure freshwater fish. In the three zones studied so far, this transition takes place over one or two kilometres.

What determines whether or not two parapatric populations become distinct species? Marine and stream sticklebacks are an amazing opportunity to investigate this question, because some pairs of marine and stream sticklebacks almost never interbreed and are therefore good species, whereas other pairs in adjacent streams seemingly mate at random. I have two broad questions: 1) do marine-stream pairs often have similar types of reproductive isolation? For example, Jeff McKinnon showed that there is often strong size assortative mating between marine and stream fish, but that may not occur in every stream, especially when the fish are similar sizes. 2) Is there any correspondence between the strength of reproductive isolation and the environment where the species meet? One potentially important factor is the presence or absence of an environmental transition where the two populations meet: some marine-stream pairs meet at the boundary between salt and fresh water, whereas others meet in small tributaries to large rivers, where all the water is fresh. I hope to get data on hybrid zones around the Strait of Georgia in summer 2007.

© 2012 Tim Vines