The secret life of invaders

Invasive lionfish. (Wikimedia Commons:  LASZLO ILYES, Jacopo Werther)

So I have this pet theory. And damn if the evidence doesn’t seem to be piling up.

Am I living in the bubble of my own google alerts? Possibly.

I’m an evolutionary ecologist and invasion biologist, and (surprise!) my pet theory is about invasive species (and by that I mean, species introduced to novel habitats by humans, which detrimentally affect the habitats they invade). I’m interested in invasive species, not just for the dramatic impacts they can have on human and natural systems in their own right, but because, in the game of global change, they are #winning.

Every species, to some degree or another, is facing the challenge of the rapid rise in global temperatures, and all the knock-on effects that can have. Invasive species will see that bet, and raise you change in (potentially) every other environmental factor AND biotic interaction. And they will go home with all of your chips, thank you very much. How do they manage it?

Here’s where my pet theory comes in – What if they are all hybrids of some degree? Elstrand & Schierenbeck (2000), and later Schierenbeck & Elstrand, (2008) proposed hybridization as a catalyst for invasive evolution. Hybridization, when it works (and it doesn’t always, Dormontt et al. 2017), has a lot of potential upsides in the novel environment/global change/non-equilibrium context.

Hybridization gives the new kid in town a chance to pick up locally adapted alleles from native relatives (Pfenning et al 2016). Mixing gene pools can shake off homozygous deleterious allele combinations, and increase genetic variation upon which selection can act in a novel environment.

“Hybridization can promote range expansion via its genetic effects. (a) Two species of fish (indicated by the different shapes and genotypes) that occupy different habitats (differential shading) hybridize and produce viable and fertile F1 offspring, which (b) later backcross to one parental species. (c) As a result of introgression, one of the parental species acquires an allele (indicated as ‘a’) that enables adaptation and expansion into the other environment. Allele ‘a’ could encode for a key functional trait that is already adaptive in that environment. Alternatively, allele ‘a’ could represent additional genetic variation that interacts with other loci to take the species to a different adaptive optimum for that environment (see text).” From Pfenning et al., 2016

Heterosis (a.k.a. hybrid vigor) can give the F1 progeny of a cross a real va-va-voom, resulting in increased biomass and reproduction. In some cases this heterotic effect can be fixed in later generations, for example, through allopolyploidy.

When two species come together, beautiful things can happen for their progeny, including the transgressive ability to survive in habitats novel to either parent (Rieseberg et al., 2007). Of course, if you scratch at this sort of itch hard enough, you get down to the ever-looming question, what even is a species? And nothing makes a speciation biologist’s eyes roll back into their head so fast as the inkling of a debate about species concepts.

via GIPHY

But we can sidestep the gnarly ‘if they cross are they really separate species?’ question, because hybridization occurs along a gradient of genetic differentiation, and even intra-species hybridization, crossing between structured populations, can be enough to get the benefits of heterosis and potentially increased invasiveness (van Kleunen et al. 2015a). It is so reliable that crop seed producers routinely sell F1 seeds for maximum crop production (Fu et al. 2014).

This origin story for most invasive species may be more reasonable then you might first expect. If humans managed to transport a given species from its native range once, then odds are, it could happen more than once. And if this transportive activity is happening in one part of its native range, then it’s quite possible it is happening in multiple parts of its native range. Because humans get around. And that’s all you need to set the stage for intra-species hybridization. So how many invasive species have recent hybrid ancestry? This should be testable hypothesis, right?

It seems like a lot, and it seems like the more we look, the more we find. But we are hampered by our ignorance of natural history. Every few years another meta-analysis takes a crack at pulling patterns out of databases of invasive species and their traits (van Kleunen 2010, Razanajatovo et al. 2016), every year with a larger dataset. And so far, our progress at describing the characteristic traits of an invader is hard-won and not entirely.

And we have tried, friends. Oh man, have we tried. But such databases are only as good as the species level studies from which they are built. And a lot of these species haven’t  been studied very well. In many cases, their biology and natural history are vague, at best. For example, if you are trying to figure out if the ability to self-fertilize is a trait characteristic of an invader, essential to the whole invasion process, and the best info you can find for a species is an assertion from a paper a several decades old saying it is “likely to be self-compatible”… well, that’s not the level of precision one would hope.

Approximately 13,000 plant species, or the equivalent of the entire flora of Europe, have become globally naturalized outside their native range through human actions (van Kleunen et al 2015b). And yet it is difficult and a lot of work to scrape together even the most basic of biological information, like whether or not a species has the ability to self-fertilize (Razanajatovo et al. [2016] managed to get this information for ~500 naturalized species, to address the selfing question. TL;DR: You’d think the ability to self would be handy, as a stranger in a strange land, and it looks like it is). Given that amount of noise, we rapidly lose our ability to detect a signal. ‘Garbage in, garbage out’, as my PI told me as an undergrad.

So to understand the patterns in something as relatively subtle as intra-specific hybridization we need more natural history and genetic data. Sometimes with more data, things we thought were hybrids turn out not to be (Owens et al. 2016). And some (a lot of?) times it goes the other way (Wilcox et al. 2018).

 

References

Dormontt, E. E., Prentis, P. J., Gardner, M. G., & Lowe, A. J. (2017). Occasional hybridization between a native and invasive Senecio species in Australia is unlikely to contribute to invasive success. PeerJ, 5, e3630. doi:10.7717/peerj.3630

Ellstrand, N. C., & Schierenbeck, K. A. (2000). Hybridization as a stimulus for the evolution of invasiveness in plants? Proceedings of the National Academy of Sciences, 97(13), 7043–7050. doi:10.1073/pnas.97.13.7043

Fu, D., Xiao, M., Hayward, A., Fu, Y., Liu, G., Jiang, G., & Zhang, H. (2014). Utilization of crop heterosis: a review. Euphytica, 197(2), 161–173. doi:10.1007/s10681-014-1103-7

van Kleunen, M., Weber, E., & Fischer, M. (2010). A meta-analysis of trait differences between invasive and non-invasive plant species. Ecology Letters, 13(2), 235–245. doi:10.1111/j.1461-0248.2009.01418.x

van Kleunen, M., Dawson, W., Essl, F., Pergl, J., Winter, M., Weber, E., … Pyšek, P. (2015b). Global exchange and accumulation of non-native plants. Nature, 525(7567), 100–103. doi:10.1038/nature14910

van Kleunen, M., Röckle, M., & Stift, M. (2015a). Admixture between native and invasive populations may increase invasiveness of Mimulus guttatus. Proc. R. Soc. B, 282(1815), 20151487. doi:10.1098/rspb.2015.1487

Owens, G. L., Baute, G. J., & Rieseberg, L. H. (2016). Revisiting a classic case of introgression: Hybridization and gene flow in Californian sunflowers. Molecular Ecology. doi:10.1111/mec.13569/pdf

Pfennig, K. S., Kelly, A. L., & Pierce, A. A. (2016). Hybridization as a facilitator of species range expansion. Proc. R. Soc. B, 283(1839), 20161329. doi:10.1098/rspb.2016.1329

Razanajatovo, M., Maurel, N., Dawson, W., Essl, F., Kreft, H., Pergl, J., … van Kleunen, M. (2016). Plants capable of selfing are more likely to become naturalized. Nature Communications, 7, 13313. doi:10.1038/ncomms13313

Rieseberg, L. H., Kim, S.-C., Randell, R. A., Whitney, K. D., Gross, B. L., Lexer, C., & Clay, K. (2007). Hybridization and the colonization of novel habitats by annual sunflowers. Genetica, 129(2), 149–165. doi:10.1007/s10709-006-9011-y

Schierenbeck, K., & Ellstrand, N. (2009). Hybridization and the evolution of invasiveness in plants and other organisms. Biological Invasions, 11(5), 1093–1105. doi:10.1007/s10530-008-9388-x

Wilcox, C. L., Motomura, H., Matsunuma, M., & Bowen, B. W. (2018). Phylogeography of Lionfishes (Pterois) Indicate Taxonomic Over Splitting and Hybrid Origin of the Invasive Pterois volitans. Journal of Heredity, 109(2), 162–175. doi:10.1093/jhered/esx056

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About Kathryn Turner

I'm an Eberly Postdoctoral Fellow in the College of Science at Penn State in the labs of Dr. Jesse R. Lasky (Biology) and Dr. George H. Perry (Anthropology). I'm interested in what happens when humans mess with plants, by spreading them around all willy nilly. Invasive species are my Moriarty. In my free time, I grow things, pickle them, brew beer with them, compost what's left.
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