Invasion by land, river, and sea

One obvious effect of climate change will be the spread of invasive species and the subsequent ecological, commercial, and health repercussions.  Therefore, studies that address the patterns of colonization and possible underlying genetic mechanisms that may lend to being a successful invader are worth paying attention to IMHO.  Three papers have come out recently that each focus on genetic components of invasive species in either the terrestrial, marine, or freshwater realm. 

First up, Sherpa et al. examined the role genetic admixture plays in the invasion biology of the Asian tiger mosquito, Aedes albopictus, the most invasive mosquito species in the world, with established populations now on every continent save Antarctica.  It is a vector for dengue, zika, and other nastiness so understanding where host invasions originated, how fast they can spread, and adaptive advantages of founder populations has important implications for epidemiology and vector and disease biology. The authors looked at A. albopictus populations from Reunion Island and Europe.  Tropical Reunion Island, with both a wetter and a drier coast represents an older invasion (>100 years). 

Europe was first colonized by A. albopictus 40, then 30 years ago and some populations established only within the last dozen years. The authors were interested in knowing if populations from Reunion Island and Europe are connected (previous studies suggested maybe) and how genetic diversity levels compared between Europe and Reunion Island and among populations within each region.  Using standard methods (de novo assembly of loci via Stacks, population clustering via STRUCTURE, maximum likelihood tree building via RAxML, genetic distances, and pairwise F_ST), they show that there is no genetic connectivity between Reunion Island and Europe, though there are daily movements of people and cargo between those two regions.  The genetic distinctiveness between these two regions indicate that the mosquito invasions happened independently (as the historical record states) from independent sources. Genetic patterns among Reunion Island conform to the isolation-by-distance (IBD) model of differentiation, which suggests that these populations have been stable long enough to reach migration-drift equilibrium.  Furthermore, there was no evidence of differentiation between the wetter and drier coasts (a result that contradicted previous studies with different markers).  

Strikingly, the F_IS values were consistent with those expected from a species with low dispersal ability. Conversely, European populations showed no IBD signal and the oldest populations (Italy, Albania) were not different from the edge of the invasion (France, Slovenia). Genetic patterns in Europe suggested that Albania was colonized first but that bottlenecked population remained isolated from the rest of the European invasion while maintaining a low level of genetic diversity. An introduction of A. albopictus in Italy in 1990 led to subsequent expansions into the rest of Europe via a bridgehead effect where an introduced population becomes the source of secondary introductions begetting a chain reaction of sorts. A horrifying feature of human-mediated spread of invasive species is how they undergo rapid, long-distance jumps as opposed to a diffusion pattern of spreading.  This brings genetically different populations into contact where admixture occurs, thus providing a pool of novel genetic combinations to continue to the reign of terror, as exemplified in the Asian tiger mosquito.

[As an aside, I was struck by the clear methods section in this paper.  The analyses were straightforward and easy to follow. The authors took extra space to explain what would be expected or why they chose one methodology over the other.  Frankly, I’m surprised there wasn’t pushback to trim the methods of anything remotely extraneous, but I’m grateful it got included.  In the age of increasingly reductionist methods, I applaud extra detail that does not require the reader to infer or extrapolate.]

Next we have a study that focused on the formidable lionfish. Anyone who’s been scuba diving in the Gulf of Mexico or Caribbean in the last decade or so knows that these aggressive aquarium fish native to the Indo-Pacific are swiftly staking claim to many coral reef habitats and outcompeting/consuming pretty much every fish in sight. Can we all just agree to not dump our unwanted pets into the outdoors, especially if they are VENOMOUS?

Along with the typical demographic hypotheses, this paper sought to identify a gene or set of genes under selection in the invading population, which may be conferring adaptive advantage to lionfish that have found themselves in novel niches. Along with population patterns, Bors et al. searched for loci by looking for sections of the genome with larger F_ST values as compared to their neighbors.  Of the 24 loci identified as putatively under selection, seven were identified by BLAST and three were flagged as particularly interesting due to their function: learning and memory, gamete maturation, and cell division and growth.  As with most studies on non-model organisms, the results were hampered by what little genomic resources there are available to facilitate identification of genes.  Nevertheless, it’s an intriguing result and sets the stage for future studies targeting those specific genes. The demographic patterns were not surprising – genetic diversity was inversely correlated with geographic distance from the point of initial introduction in Florida.  However, an important insight from this paper worth mentioning is the attention to sampling needed in invasive species studies.  In situations where the invasion happened very recently, and many age classes may be present, which may confound interpretations of when and how the invasion is progressing.  This study also introduced me to the term allele surfing, which is the process of a rare allele rising to high frequency/fixation near the edge of the expansion of a population due to repeated founder effects.  Learning!

 My favorite example of interesting biological invasions, though, is the marbled crayfish.  These anomalous creatures have gotten much attention of late (see here and here and especially McSWEENEY’S take here, which coins the phrase “asexual Aphrodite” (stellar band name)).  The prevailing theory is that about 25 years ago, two distantly related slough crayfish (native to Florida) mated in an aquarium in Germany.  However, one of the two had an autopolyploid gamete, resulting in a triploid offspring.  Under most circumstances, this would be an evolutionary dead end lost to the annals of time, but this genomic duplication conferred an advantageous adaptation: obligate parthenogenesis. Voila! Much like Dr. Frankenstein flipping a switch in his lab, a new, all female, clonal evolutionary trajectory was created instantaneously. Since their genesis in 1995, marbled crayfish have spread across Europe and Africa eating everything in sight (detritus, fish, insects). First introduced in Madagascar in 2005, they now occupy 100,000km² and threaten several native crayfish species. Oh, and they can be carriers of the dreaded crayfish plague as well. This genome is one of the only decapod crustacean genomes to be sequenced (!!), one of the few from asexually reproducing animals, and perhaps the only one from an asexual reproducer with the evolutionary history of a quarter century.  As the marbled crayfish persists, the evolution of its genomic architecture will be fascinating to track.  Unfortunately, it will be at the expense of native crayfish.

Bors, EK, Herrera, S, Morris, JA, Shank, TM. Population genomics of rapidly invading lionfish in the Caribbean reveals signals of range expansion in the absence of spatial population structure. Ecol Evol.2019; 9: 3306– 3320. https://doi.org/10.1002/ece3.4952

Gutekunst J, Andriantsoa R, Falckenhayn C, Hanna K, Stein W, Rasamy JR, Lyko F. Clonal genome evolution and rapid invasive spread of the marbled crayfish. Nat Ecol Evol. 2018;2:567–73.

Sherpa, S. , Blum, M. G., Capblancq, T. , Cumer, T. , Rioux, D. and Després, L. (2019), Unraveling the invasion history of the Asian tiger mosquito in Europe. Mol Ecol. Accepted Author Manuscript. doi:10.1111/mec.15071