How diversity creates itself - cascades of new species among flies and parasitic wasps

Not Exactly Rocket Science
By Ed Yong
Feb 9, 2009 7:30 PMNov 5, 2019 2:03 AM

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This is the second of eight posts on evolutionary research to celebrate Darwin's bicentennial.

What do you get when one species splits into separate lineages? Two species? Think bigger...

When new species arise, they can set off evolutionary chain reactions that cause even more new species to spring forth - fresh buds on the tree of life create conditions that encourage more budding on different branches.

Biologists have long suspected that these "cascades of speciation" exist but have struggled to test them. Enter Andrew Forbes from the University of Notre Dame - his team of has found a stunning new proof of the concept by studying a fruit fly called the apple maggot (Rhagoletis pomonella) and the parasitic wasps that use it as a host.

Contrary to its name, the apple maggot's natural host is not apples - it's hawthorn. The fly only developed a taste for apples about 150 years ago, when the fruit was first introduced to North America. This culinary switch has created two races of apple maggot - one that eats hawthorn and another that eats apples. Even though they are often found in the same place, the two races don't mix and they don't breed together. They are well on the road to becoming separate, genetically distinct species.

And so are their parasites. A wasp called Diachasma alloeum specialises in attacking apple maggots. It lays its eggs inside the fly larvae, and its grubs eat the victim from the inside out. Forbes found that the wasp has also started to form separate races that don't crossbreed with one another, even though they have overlapping ranges. By adapting to new host plants, the flies inadvertently set up barriers that separated their respective parasites from one another. Now, the wasp, like its hosts, are also on the way to becoming separate species. It's a fantastic example of diversity bringing itself about.

Forbes studied these changes by collecting thousands of samples of both flies and wasps from the eastern United States. His team studied both races of apple maggot along with two closely related species, the blueberry maggot (R.mendax) and the snowberry maggot (R.zephyria). You'd find it almost impossible to tell the difference between them by sight but these species are indeed genetically distinct.

Each maggot eats the fruit of a different plant, and each plant bears fruit at different times of the year. Because the flies have just one generation per year and live short lives, adults of one species rarely buzz around at the same times as those of the others. It's shift-working on a massive scale - all the flies may live in the same place, but time separates them and thus, their genes.

This chronological separation is boosted by a geographical one. The flies stick to the fruit that they ate as maggots, by following their distinctive smells. They mate there and lay their eggs there - another barrier that prevents the genes of different races or species from mixing.

The wasp D.alloeum targets flies from all four host plants and Forbes found that it is influenced by the same barriers that have cordoned off the flies into mutually exclusive populations. By sequencing DNA from various positions in the wasps' genomes (and those of their mitochondria), he showed that some genetic variations consistently turned up in some wasps but not others, depending on which flies they attacked.

The wasps had effectively splintered into apple, hawthorn, blueberry and snowberry populations, just as their hosts had done. The mitochondrial sequences revealed that these splits were relatively recent affairs, but even now, there is little genetic flow between the different sub-groups. And that was due to the same timing issues that have divided the flies.

By observing wild wasps, Forbes found that they do indeed mate and lay eggs near the fruits of their chosen hosts. They have a life-long affinity for the distinctive smell of their fruity birthplace. Using Y-shaped chamber with smells pumping down one arm, Forbes shown that D.alloeum is drawn towards the odour of its preferred fruit and no others. It's more likely that this preference is inherited rather than something the wasps learn as larvae. After all, they are laid inside the flies and pupate as soon as they burst out - they're never actually in contact with the fruit itself.

The wasps are not just separated in space, but also in time. The fruits ripen at different times, the flies emerge to synchronise with the fruit and the wasps emerge to synchronise with the flies. They too have short life-spans of about two weeks and just one generation ever year, so adults from populations based on different fruits have few opportunities to meet. Forbes even found that these timing differences in the wasp life-cycles may be influenced by the very genetics variations that he identified earlier.

The expansion of the Rhagolettis flies into species and races that eat different fruits has triggered a parallel expansion among the wasps that exploit their bodies. The smell and timing of different fruits act as invisible barriers that keep different populations of both flies and wasps apart.

Forbes even suggests that the effect may work both ways. It's possible that the wasps themselves have provided the impetus for the flies to exploit new fruits in the first place. Those that did so would find themselves with a big advantage in a new environment free of enemies. But that itself creates a fresh niche for the wasps to exploit, and they too diverge to make the most of the new riches.

This is the clearest example yet of a "cascade of speciation", of diversity creating more diversity. It is absolutely not the only one. Just think about these statistics. There are more plant-eating insects than any other life form on earth and they are plagued by hordes of parasites that co-opt their bodies. In fact, Forbes cites that one in five of all insects are probably parasitic wasps. Perhaps these ripples of divergence are the very reason why these insects groups are so remarkably varied. As Forbes says, "There is a world of opportunity for sequential speciation in nature."

Reference: A. A. Forbes, T. H.Q. Powell, L. L. Stelinski, J. J. Smith, J. L. Feder (2009). Sequential Sympatric Speciation Across Trophic Levels Science, 323 (5915), 776-779 DOI: 10.1126/science.1166981

Images: Fly by Rob Oakleaf; others by Andrew Forbes

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