Molecular ecologists — and molecular ecology — at Evolution 2019

The Providence skyline. (Flickr: Timothy Burling)

June means summer is well underway in the northern hemisphere, and those of us tied to the academic calendar are off to fieldwork, buckling down for summer teaching or grant-writing or just writing — and planning for conferences. Evolution, the joint annual meeting of the American Society of Naturalists, Society of Systematic Biologists, and Society for the Study of Evolution, is a big one for molecular ecology and molecular ecologists, and as in many years multiple contributors to this very blog will be present and presenting in Providence, Rhode Island. Here’s a quick rundown of which TME contributors and alumni will be speaking at Evolution 2019, and what events on the program schedule have us excited. Look for our coverage of the conference itself when we converge on the [checks Wikipedia] "Ocean State" on Friday, June 21.

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The state of coral: A mini-review

Coral reefs are one of the main harbingers of the climate crisis.  As such, there have been numerous studies, TED talks, Blue Planet episodes, podcasts, et cetera, about the state of corals. I’ve condensed a select few research findings for a mini-review to highlight some of the most recent results. This is by no means a comprehensive review of the coral literature, obviously.  I will, no doubt, egregiously fail to mention some rock stars who are making great strides in coral biology and conservation.  It’s a big group – both of scientists and of species.

A quick background on coral endosymbionts

Shallow water corals are considered holobionts, comprised of the host coral, endosymbiotic dinoflagellates (often referred to colloquially as zooxanthellae), bacterial and archaea communities. The endosymbionts provide the fixed carbon for the coral via photosynthesis.  When water temperature increases above average for a prolonged time, the endosymbionts are expelled from the coral polyps, leaving bleached coral behind. Corals can rely upon heterotrophy to get their nutrients and fixed carbon, but this is not sustainable over long stretches of time. They can reuptake endosymbionts and recover if temperatures return to normal in a short enough time span.  Most corals obtain their endosymbionts from the environment (horizontally) either during their larval stage in the water column or shortly after settling. Others inherit endosymbionts vertically from their parents. The most reported and studied coral endosymbionts historically have belonged to the genus Symbiodinium, but a recent revision has split the several clades within the genus into seven distinct genera.

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Hybridization in the depths of the last glacial period created a world-conquering clover

White clover, Trifolium repens, in a Los Angeles city park, a hemisphere away from the glacial refugia where it originated. (jby)

Plants’ flexibility with the structure of their genome — able to cope with proliferating transposons, whole-genome duplications, or even acquisition of complete sets of chromosomes from another species — is a big source of evolutionary novelty. Duplication of a single gene allows the duplicate and its template to evolve new functions; adding a whole additional genome provides that much more raw material. That may be the secret of the success of one worldwide weed we’ve seen featured on this blog before, Trifolium repens, or common white clover. A new paper in The Plant Cell delineates two fairly intact progenitor genomes within the T. repens genome, and reconstructs the history of an evolutionary mashup that created a wildflower you can very likely find by simply stepping outside and walking to the nearest well-watered lawn.

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Introducing Molecular Ecology Spotlight

Today, the Molecular Ecology journals are launching a new venue for highlights and behind-the-scenes looks at the research they publish. Molecular Ecology Spotlight fills a niche as the official blog of Molecular Ecology and Molecular Ecology Resources, publishing author summaries and interviews linked to noteworthy new papers in the journals — and a Twitter feed that will broadcast all new papers as they’re published.

The new blog is a project of the Junior Editorial Board, formed last year with early-career researchers who were recognized in the Harry Smith Prize competition. The goal is that this will provide another way to follow research results from the journals, and context and background for papers of particular interest; where The Molecular Ecologist has always defined itself as a forum for the field of molecular ecology writ broadly, Molecular Ecology Spotlight will, as the name implies, shine a light on the best work in Molecular Ecology and Molecular Ecology Resources specifically.

You can find Molecular Ecology Spotlight at molecularecologyblog.com, and on Twitter at @molecology.

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Go north, young salamander

Plethodon shenandoah (Wikimedia Commons)

Shenandoah salamanders are a case study in restricted distributions, known only from three mountainsides in Shenandoah National Park, in the Appalachian Mountains of Virginia. What’s keeping them in such a restricted range? A new paper in the journal Ecology and Evolution aims to answer that question using population genetics.

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Bigger bees bumble by barriers, end up with lower population genetic differentiation

Look at the dispersal ability on that lad! What an absolute unit. (Flickr: Viv Lynch)

Population structure is the core of ecological genetics, as it’s practiced today. Genetic differentiation between populations in different places is our null hypothesis and one of our most widely used indirect signals that environmental factors are impacting the evolution of those different populations. Oh, and it’s also a first step to the origin of new species.

The huge body of published datasets testing for population structure is a great resource for synthetic work, that identifies broad general patterns about population genetic processes. Last year we saw one such study link locomotion mode and genetic differentiation — confirming that bird populations are less likely to differentiate, given a particular geographic distance, than populations of land-bound vertebrates. Now, freshly out in Molecular Ecology, we have a similar project in a more specific taxonomic scope: bees.

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Move or adapt to changing climate? These chipmunks have had to do both

Tamias alpinus (Flickr: Eric Sonstroem)

Climate change threatens to land many, many species in conditions for which they’re not adapted — too warm, too dry, too stormy, too flood-prone — and traditionally the ways that living things might respond to this are framed as a choice between moving to more suitable habitat elsewhere, adapting to the new conditions in the current habitat, or dying out. These are a false choice, of course; it’s possible to move and adapt, and it’s possible that even doing both won’t be enough to avoid extinction. A new study of one rare chipmunk in the Sierra Nevada mountains pinpoints exactly such a case.

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Scott Edwards awarded the 2019 Molecular Ecology Prize

The 2019 Molecular Ecology prize has been awarded to Scott Edwards for an illustrious career that has combined rigorous scientific achievement with a long and consistent record of mentoring and promoting early-career scientists. Proficient at both empirical and theoretical studies, Edwards has made important contributions to coalescent modeling, phylogeographic inference, immunogenetics and other connections between genotype and phenotype, and the often-misunderstood difference between gene trees and species trees in nature, as well as many more specialized contributions to ornithology. Countless people from around the world have benefited from his work over many decades to support junior scientists and to promote diversity at all levels of the scientific enterprise.

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Nominations open for the 2019 Harry Smith Prize

The editorial board of the journal Molecular Ecologyis seeking nominations for the Harry Smith Prize, which recognizes the best paper published in Molecular Ecologyin the previous year by graduate students or early career scholars with no more than five years of postdoctoral or fellowship experience. The prize comes with a cash award of US$1000 and an announcement in the journal and in the Molecular Ecologist.  The winner will also be asked to join a junior editorial board for the journal to offer advice on changing research needs and potentially serve as a guest editor. The winner of this annual prize is selected by the junior editorial board.

The prize is named after Professor Harry Smith FRS, who founded Molecular Ecology and served as both Chief and Managing Editor during the journal’s critical early years. He continued as the journal’s Managing Editor until 2008, and he went out of his way to encourage early career scholars. In addition to his editorial work, Harry was one of the world’s foremost researchers in photomorphogenesis, where he determined how plants respond to shading, leading to concepts such as “neighbour detection” and “shade avoidance,” which are fundamental to understanding plant responses to crowding and competition. More broadly his research provided an early example of how molecular data could inform ecology, and in 2008 he was awarded the Molecular Ecology Prize that recognized both his scientific and editorial contributions to the field.

Please send a PDF of the paper you are nominating, with a short supporting statement (no more than 250 words; longer submissions will not be accepted) directly to Nick Fountain Jones (nfountainjones@gmail.com) by Friday 31 May 2019. Self-nominations are accepted.

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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 FST), 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 FIS 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 FST 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.

left: Asian tiger mosquito, Top right: lionfish, Bottom left: marbled crayfish, Bottom right: author’s extrapolation of the inevitable.

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

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