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The Mystery of the Missing Salmon-Trout Hybrids

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Study author Matt Gage holds a male salmon in the lab before returning it to the river. (Photo credit: Matt Gage)

Study author Matt Gage holds a male salmon in his lab before returning it to the river. (Photo credit: Matt Gage)

When trying to pass genes on to future generations, mating with a different species is generally the wrong way to go. Most attempts to mate between species fail. Those that succeed often result in offspring that can’t reproduce themselves. (You’ve all met the mule).

Luckily, there are all sorts of barriers that keep animals from mating with the wrong species. Eastern and western skunks share the Great Plains, but can’t mate together because they breed during different seasons. Female green tree frogs avoid mating with a closely related neighboring species by listening for differences in their call frequencies. Two millipede species may try to mate together, but attempts always fail because the necessary body parts just don’t match up.

These barriers—formed by time, behavior, or mechanics—are all clear to the observer. Other barriers, however, are equally formidable, but hide just out of view.

Take Atlantic salmon (Salmo salar) and trout (Salmo trutta). Until recently, the exact obstacle preventing these species from regularly hybridizing was a mystery. We know that these fish share many of the same rivers and have partially overlapping breeding seasons. We also know that they do at times attempt to mate. And from lab studies, we know that they are fully capable of reproducing together.

Yet in most river systems there are relatively few salmon-trout hybrids to be had. With no clear barrier in sight, what keeps these species divided?

Sarah Yeates, a scientist at the University of East Anglia, and colleagues say the answer is in the ovarian fluid. This protein-rich solution covers eggs as they lay on the river bottom awaiting fertilization. The competitive ability of sperm to move through ovarian fluid matters because female salmon and trout may spawn with multiple mates. The quicker a sperm can move through the ovarian fluid, the better the odds of fertilizing the egg before a competitor has the chance.

In their paper published online this summer in the journal Evolution, Yeates and colleagues show through a series of in vitro fertilizations that salmon and trout sperm each have a competitive edge when swimming through their own species’ ovarian fluid.

Egg batches incubating (Photo credit: Matt Gage)

Egg batches incubating (Photo credit: Matt Gage)

The authors identified the importance of this solution by first isolating it from batches of salmon and trout eggs. They then placed the eggs in beakers and bathed them in either ovarian fluid from the eggs’ own mother or from a fish from the other species. They then introduced a mixture of salmon and trout sperm to each batch of eggs and allowed the eggs to develop. Finally, using paternity testing they identified which species was most successful at fertilizing in each of the egg-ovarian fluid combinations.

Amazingly, whether an egg and sperm belonged to the same species had little influence on fertilization success. Instead, the type of ovarian fluid bathing the eggs made all the difference. Trout sperm were most successful at fertilizing in trout ovarian fluid and salmon sperm were most successful in salmon ovarian fluid.

Biologists widely recognize that females of many species can encourage fertilization by the sperm that result in the healthiest offspring. Actually identifying the tools a female uses to choose that sperm, however, is quite tricky. This study suggests that for these fish species, differences in ovarian fluid between species can help females promote the best sperm.

It’s tempting to look at these results and conclude that ovarian fluid in salmon and trout evolved in response to the threat of mating with the wrong species. Even though salmon and trout can reproduce together, they each have a different number of chromosomes, so their hybrids have genetic incompatibilities that don’t bode well for continuing the family line. Natural selection, then, might strongly favor females that produce ovarian fluid that encourages sperm from their own species over others.

It’s also possible, however, that salmon and trout each independently evolved fine-tuned sperm and ovarian fluid interactions, and any attempt to reproduce this relationship across species falls short.

Teasing apart these two explanations is the authors’ next step. But whatever its root cause, we now know the ovarian fluid barrier is responsible for keeping the line between these fish species a lot less blurred. The mystery of the missing salmon-trout hybrids is solved.

References:

Campbell, N.A., Reece, J.B., Taylor, M.R., Simon, E.J., and Dickey, J.L. (2008) Concepts of Species, Chapter 4.2. In: Biology Concepts and Connections (6th Edition)

Höbel, G. and Gerhardt, H.C. (2003) Reproductive character displacement in the acoustic communication system of green tree frogs (Hyla cinerea). Evolution. (57) 894-904.

Tanabe, T. and Sota, T. (2008) Complex copulatory behavior and the proximate effect of genital and body size differences on mechanical reproductive isolation in the millipede genus Parafontaria. The American Naturalist. (171) 692-699.

Yeates, S.E., Diamond, S.E., Einum, S., Emerson, B.C., Holt, W.V., Gage, M.J.G. (2013) Cryptic choice of conspecific sperm controlled by the impact of ovarian fluid on sperm swimming behavior. Evolution. doi:10.1111/evo.12208

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