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Lionfish: the perfect invader

The invasion of the Caribbean by Indo-Pacific lionfishes happened seemingly overnight. In the early 2000s, the first papers were published about lionfish sightings in places like Florida, half a world away from their native range—by 2010, they were almost everywhere in the Caribbean, and even now, they continue to expand the edges of their invasive Atlantic range. The naïve fish on Caribbean reefs, where lionfish did not previously occur, were decimated by this voracious predator. Populations plummeted and some fishes got dangerously scarce.

When these alien fish appeared, very little was known about their ecology or evolutionary history. Christie Wilcox, then a PhD student at the University of Hawaii, wanted to work on the genetics of the invasive lionfish Pterois volitans. Maybe by looking at their genes, Christie might help managers understand these beautiful, mysterious fish. Genetic studies could reveal the source population to help understand why the invasive fishes spread so fast, grow so quickly, and become so large.

She never did find the source population for the invasive lionfishes. Instead, her work uncovered something bigger: the invasive species P. volitans was a hybrid.

There is an old saying that the big scientific discoveries aren’t “Eureka!” moments but rather “That’s funny…” moments. It certainly fits in our case; we didn’t set out to find hybrid lionfishes dominating the Atlantic invasion. Rather, they found us, appearing suddenly and unexpectedly in our data.

At first, we had only managed to get a few lionfish specimens. We hoped to create a phylogenetic tree of the lionfish subfamily Pteroinae, but to do that, we needed to find variable DNA sequences that could separate all of the different species, including close relatives like Pterois volitans and Pterois miles (both of which have been detected in the invasive range). We started testing genetic markers thanks to generous DNA donations from David Wilson Freshwater from the University of North Carolina at Wilmington. While it was fairly straightforward to find mitochondrial DNA markers that were different between the species, we struggled to find any difference in the nuclear genome. We tried dozens of genetic loci, but couldn’t find any consistent differences between those two species.

Christie holding a juvenile lionfish from the invasive range. Photo Credit: Christie Wilcox.

Then, a few tissue specimens from the Pacific native Pterois lunulata, arrived from the Biodiversity Research Center, Academica Sinica in Taiwan. When we sequenced the different gene regions for those samples, a strange pattern emerged. For mitochondrial markers, the P. lunulata samples looked like the invasive P. volitans, but for several of the nuclear markers, they were clearly distinct. When we constructed phylogenetic trees, the few P. volitans samples we’d sequenced jumped from P. miles to P. lunulata depending on the genetic locus.

Surprised by these results, we sought out more samples. Lucky for us, Hiroyuki Motomura at the Kagoshima University Museum in Japan, and Mizuki Matsunuma, now at Kochi University, were also looking into the same lionfish group. They had collected hundreds of lionfishes from a range of species, discovering several new species in the process. It was the treasure trove of genetic and morphological data that we needed to understand why the specimens seemed so strange. Collaborating with them, we sequenced one mitochondrial locus (a portion of the cytochrome oxidase gene) and two nuclear introns for over 200 lionfishes. That’s when it became clear: P. volitans consistently shared DNA with two other species of lionfishes: its presumed sister species P. miles in the Indian Ocean, and a lineage comprised of two Pacific species P. lunulata and P. russellii.

The finding that closely related species hybridize once in awhile is not remarkable. However those two lineages have been separated for several million years, based on the mitochondrial molecular clock—more than long enough to be considered separate species. It was as if the entire species of P. volitans was made from the mixing of these other species. We found even more evidence for hybridization when we looked at the animals themselves. Those that were intermediate at the genetic level also had intermediate morphological characteristics like fin ray numbers. The correlation of genotype and phenotype strongly indicated hybridization.

Hybridization was once considered rare in the marine realm, but over time, we’ve seen many examples of hybridization between marine fishes. Species split at known barriers—like P. miles and P. lunulata/russellii, which are found in the Indian and Pacific Oceans, respectively—are particularly prone to such interspecies mingling. But so far, most hybrids are restricted to a thin range along the Indian/Pacific boundary. The hybrid P. volitans has a vast range across the Western Pacific. Given the success of P. volitans in its native range, these lionfishes may be getting a benefit from their mixed genes, a phenomenon called heterosis or hybrid vigor. Could the Atlantic invader be a superfish?

Lionfish Pterois miles from the Red Sea, one of the two species that make up the hybrid invader in the Atlantic. Photo Credit: Tane Sinclair-Taylor. Used with permission.

Armed with this new information from the native range, we took a fresh look at the invasive Atlantic range. Nearly all of the invasive fishes we examined from the coast of North Carolina were hybrids.

If our findings are correct, then they suggest that to really understand the invasive lionfish, we can’t just look at similar lionfishes. We have to look at the biology and ecology of the lionfishes that served as the source of the invasive population—a source which remains a mystery.

Our findings also might explain why the lionfishes in the invaded range are doing so well. The invader is a fast growing, highly fecund, generalist predator armed with venomous spines, placed into a habitat free of its normal parasites, predators, and competitors. The combination of naïve prey in the invaded range, and hybrid vigor, may have produced the perfect invasion, a terrifying precedent in the annals of invasion biology.

Featured image by bachstroem. CC0 public domain via Pixabay.

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