Summary from the authors: Detection of environmental and morphological adaptation despite high landscape genetic connectivity in a pest grasshopper

Male and female Phaulacridium vittatum. Photo credit: Sonu Yadav.

The Australian native grasshopper, Phaulacridium vittatum, known as the wingless grasshopper, is a common pest of pastures and crops in Australia, with outbreaks recorded every four or five years. With climate change and the expansion of agricultural land use, there is concern that grasshopper outbreaks could increase in frequency and severity. We used both neutral analysis of landscape genetic resistance combined with detection of selection using Environmental Association Analysis (EAA) to investigate common and disparate environmental drivers of  genetic dispersal and local adaptation in this grasshopper pest. With SNP data collected across a 900km gradient, we found that gene flow was best predicted by temperature, with only urban areas and water bodies limiting genetic dispersal. Although there was considerable admixture across the study area, local adaptation was evident and similarly driven by temperature, with additional evidence of morphological adaptation (body size and stripe polymorphism). Gene annotations revealed functions linked to UV shielding, and detoxification processes. Our study indicates that P. vittatum has high potential to adapt to heterogenous environments under high gene flow, and that temperature is the primary driver of both neutral and adaptive genetic structure. Thus, P. vittatum may become a more serious pest in the future as temperatures become warmer, and agricultural land use expands. 

Yadav S, Stow AJ, Dudaniec RY. Detection of environmental and morphological adaptation despite high landscape genetic connectivity in a pest grasshopper (Phaulacridium vittatum). Mol Ecol. 2019;28:3395–3412.

Summary from the authors: Dispersal limitations and historical factors determine the biogeography of specialized terrestrial protists

The diversity and geographical distribution of plants and animals are well documented and this information was essential to understand the factors that generate biodiversity, the most famous example being Darwin and Wallace’s theory of evolution. However, we know much less about microbial diversity and distribution, and hence it is unclear if the same factors drive the diversity of large and small organisms.

Hyalosphenia papilio from Le Cachot Bog, Swiss Jura Mountains. Picture by Prof. Daniel Lahr.

Using molecular tools, we studied the distribution and diversity of a species complex of the testate (shell-producing) amoeba species Hyalosphenia papilio, a microorganism restricted to Sphagnum peatland of Eurasia and North America. H. papilio is a complex of 14 distinct molecular lineages. Based on the DNA sequences, we inferred how, where and when this diversity evolved.

Our results suggest that H. papilio evolved in western North America and subsequently colonized other regions of Eurasia and North America during interglacial periods. Colonization of Eurasia occurred most recently, possibly after the last glaciation.

The patterns we observed for H. papilio are consistent with those commonly observed for macroscopic plants and animals. This in turn suggests that microbial diversity may be much higher than currently thought and may include “relict” taxa with restricted distributions, as commonly found among macroscopic plants and animals.

Read the full article: Singer D, Mitchell EAD, Payne RJ, etal. Dispersal limitations and historical factors determine thebiogeography of specialized terrestrial protists. Mol Ecol. 2019;28:3089–3100.

Summary from the authors: Genome‐scale sampling suggests cryptic epigenetic structuring and insular divergence in Canada lynx

Wild populations are often genetically structured in complex ways due to migration, selection, and drift. In highly mobile species such as the Canada lynx (Lynx canadensis), these complexities are exacerbated due to high levels of gene flow, which can make population delimitation challenging. Previously, Canada lynx populations appeared largely undifferentiated across continental North America at neutral genetic markers, with only small fine-scale differences across the landscape being correlated with climatic gradients. This climatic structuring aroused our interest in potential epigenetic differences between Canada lynx across their range, as environmentally-induced modifications to DNA could explain geographical or morphological differences that are not apparent in neutral DNA.

A lynx stalks its prey in the Northern forests of the Canadian Yukon, bordering Alaska. Photo credit to Dr. Melanie Boudreau.

To test this hypothesis, we examined neutral genetic differences and patterns of DNA methylation between 95 Canada lynx across 4 geographical regions (Alaska, Manitoba, Québec, and an insular population on Newfoundland). We found that Newfoundland lynx were the most distinct at both genetic and epigenetic markers, consistent with what we would expect for an island population. However, despite low neutral genetic differentiation between all mainland populations, we detected stark epigenetic differences between Alaska lynx and the remaining mainland lynx. Further analyses indicated that these differences might correlate with increased energetic demands, consistent with Alaskan lynx being the morphologically largest of all in their range. Our study exemplifies the utility of epigenetic markers for assessing population structure, even in non-model systems characterized by extreme levels of gene flow. 

Summary of neutral genetic structure with SNPs (left) and patterns of DNA methylation (right) between Canada lynx, where each circle represents an individual lynx colored by geographic region. Alaskan lynx (purple) are largely undifferentiated at neutral genetic markers compared to other mainland lynx, in contrast to their epigenetic profiles. 

Read the full article: Meröndun J, Murray DL, Shafer ABA. Genome-scale sampling suggests cryptic epigenetic structuring and insular divergence in Canada lynx. Mol Ecol. 2019;28:3186–3196.

Interview with the authors: Phylogeography of a cryptic speciation continuum in Eurasian spadefoot toads

Understanding how species form, and the factors that contribute to reproductive isolation has been a long-standing goal of evolutionary biology. Cryptic radiations can provide insight into these questions. Dufresnes and colleagues investigate these questions in a cryptic radiation of Eurasian spadefoot toads (Genus Pelobates). They find a correlation between the amount of time spent in allopatry and the level of reproductive isolation between lineages experiencing secondary contact. Get a behind-the-scenes look at the research below with first author Christophe Dufresnes.

Aquatic portrait of the Common Spadefoot Pelobates fuscus. This species belongs to a cryptic speciation continuum new to science, deciphered through a fine-scaled genomic phylogeography. Credit: Edvárd MIZSEI.

What led to your interest in this topic / what was the motivation for this study? 

This study was part of my post-doc efforts to compare geographic and genomic patterns of introgression across hybrid zones from several amphibian radiations, in order to understand the pace and the genetic mechanisms of allopatric speciation. For Pelobates, we originally intended to focus only on the P. fuscus/vespertinus hybrid zone in Ukraine/Russia, but inadvertently discovered that our outgroup taxon (the traditionally-recognized P. cf. syriacus) consisted of a cryptic diversification involving several phylogeographic transitions. Instead of one contact, it turned out we could study as many as six within a single radiation. We thus seized that rare opportunity to understand the relationship between genetic divergence and reproductive isolation under natural settings, which had only been attempted in a handful of systems so far.

What difficulties did you run into along the way? 

Not much actually, except perhaps time constrains and taxonomic issues. Because we were willing to describe the new Pelobates species/subspecies discovered and use the appropriate names in our Mol. Ecol. article for clarity, we had to synchronize the peer-reviewing and publication of an accompanying paper (ZooKeys 859: 131–158). This was successful thanks to the support of the two journals and both papers were released just a few hours apart. The scientific stages per se went remarkably smoothly. Colleagues from many countries were enthusiastic to send us samples, the RAD-seq wet lab and bioinformatics performed admirably, and data analysis was straightforward. At the end, it took only about a year and a half from project initiation to publication.

What is the biggest or most surprising finding from this study? 

We were astonished by the strong divergence (>5My) between the Asian and European populations of P. cf. syriacus, and their lack of interbreeding despite parapatric (and perhaps even sympatric?) distributions near the Bosphorus. While they clearly represent two different species (coined P. balcanicus and P. syriacus), no phenotypic differences have been reported (despite several morphometric surveys), so this was not suspected. But more globally, our big finding is the very neat link between genetic divergence and admixture across phylogeographic transitions. It was beyond expectations since hybridization at contact zones often depends on local factors (dispersal constraints, etc.), which blurs the link. Such a clear relationship supports the Darwinian view of a gradual and dynamic speciation continuum, and extends it to cryptic radiations of eco-morphologically similar species.

Moving forward, what are the next steps for this research? 

We have several major follow-ups ongoing. Our Pelobates speciation genomic framework is now being implemented into multi-system comparative analyses aiming to understand how the genetic architecture of reproductive isolation evolves as speciation progresses, by re-analyzing transitions at the locus scale. In parallel, we are characterizing the homomorphic sex chromosomes of Pelobates to gauge their importance in hybrid incompatibilities. Following this research, our co-author Ilias Strachinis has now just started a PhD on Pelobates from the Balkan Peninsula to study the diversity and distribution of the new lineages unraveled. It should provide significant insights for their biogeography and conservation, notably of the mysterious Peloponnese endemic P. balcanicus chloeae.

What would your message be for students about to start their first research projects in this topic? 

Even in supposedly well-studied biogeographic regions like the Western Palearctic, do not take the established phylogenies, species delimitations and taxonomies for granted! Significant diversifications may have been overlooked, especially since previous work relied mostly on mitochondrial and poorly-informative nuclear markers, which can be deceptive to disentangle among closely-related lineages. Nowadays, RAD-seq provides affordable, powerful and straightforward resources to address many questions with a combination of population genetic and phylogenetic analyses, so it appears a tool of choice to study the phylogeography of speciation in many taxonomic groups.

What have you learned about science over the course of this project? 

That unexpected results are worth exploiting and may lead to fascinating scientific discoveries. An unthinkable amount of biodiversity still lies unnoticed right under our noses. Moreover, our study was only possible (especially in such an efficient timeframe) thanks to a great collective effort bringing together renowned teams of herpetological researchers. From my personal perspective, this human aspect emphasizes how science is best appreciated collaboratively rather than through competitive emulation, and I look forward to reiterate the experience.

Describe the significance of this research for the general scientific community in one sentence.

In cryptic diversifications, whether the continuous nature of speciation leads to discrete, reproductively-isolated entities is mostly dependent on the time they spent in allopatry.

Describe the significance of this research for your scientific community in one sentence.

Our study provides empirical evidence within a single radiation that speciation is a dynamic and reversible process where phylogeographic lineages can merge together upon secondary contact, unless a threshold of evolutionary divergence is reached (>3My in amphibians), in which case they can quickly build up reproductive isolation and become incipient species.

Read the full article here: Dufresnes C, Strachinis I, Suriadna N, et al. Phylogeography of a cryptic speciation continuum in Eurasian spadefoot toads (Pelobates). Mol Ecol. 2019;28:3257–3270.

Summary from the authors: Geography best explains global patterns of genetic diversity and post-glacial co-expansion in marine turtles

A hawksbill turtle (Eretmochelys imbricata). Photo Credit: Banco de Imagens Projeto Tamar.

Marine turtle species exhibit differences in characteristics that could affect their sensitivity to climate change, such as size, generation time, diet, and thermal preferences. Research on nesting turtles has also shown that there are often multiple maternal lineages within a species, some spanning whole ocean basins and others much more restricted. These geographic differences could also have influenced past responses to climate change. We compiled data from 23 marine turtle lineages and compared the observed data to many simulated datasets to determine whether lineages were stable, expanding, or contracting over time. We then looked at which factors best predicted past population history and genetic diversity. We found evidence for population expansion in 60% of the lineages, with the remaining lineages stable over time. A co-expansion model showed that the lineages that expanded did so in a highly synchronous manner after the last Ice Age. Geographic factors (ocean basin and range extent) were much better predictors of population history and genetic diversity than species traits. So, where you were mattered more than who you were in determining response to global warming. This can inform conservation planning for these species and other marine organisms in the face of climate change.

For the full article: Reid BN, Naro‐Maciel E, Hahn AT, FitzSimmons NN, Gehara M. Geography best explains global patterns of genetic diversity and postglacial co‐expansion in marine turtles. Mol Ecol. 2019;28:3358–3370.

Summary from the authors: Plant DNA-barcode library and community phylogeny for a semi-arid East African savanna

A DNA-barcode library is provided for the plant community of Mpala Research Centre’s semi-arid savanna ecosystem. Photo Credit: Tyler Kartzinel

African savannas represent iconic ecosystems comprising diverse plants and animals. Despite their importance to nature and people, the species that live in these ecosystems are relatively underrepresented in global biodiversity databases. To facilitate studies on the ecology and evolution biodiversity in East Africa, this international team of researchers developed a plant DNA-barcode library. We collected and identified 460 plant species from habitats across the ~200-km2 Mpala Research Centre in Laikipia, Kenya. These voucher specimens are archived at the National Museums of Kenya and the Smithsonian Institution. Based on these collections, we constructed a DNA-barcode library by sequencing 5 molecular markers from 1,781 vouchered plant specimens and generated 4,696 DNA sequences. This library increased the representation of plant DNA sequences from Africa within the Barcode of Life Database by nearly 10%. We demonstrated that these DNA barcodes are capable of discriminating between the vast majority of plant species present in this semi-arid savanna community and we used these sequences to infer a robust community phylogeny. We believe that this collection of plant voucher specimens, DNA barcodes, and the community phylogeny will support further research occurring both within this savanna ecosystem and across global biodiversity databases.

For the full article, see:
Gill, BA, Musili PM, Kurukura S, et al. Plant DNA-barcode library and community phylogeny for a semi-arid East African savanna. Mol Eco Resour. 2019;19:838-846.

Interview with the authors: Parallel introgression and selection on introduced alleles in a native species

Species introductions serve as a natural laboratory to study introgression and selection. In a recent paper in Molecular Ecology, Rachael Bay and colleagues use introduced rainbow trout and native cutthroat trout to study hybridization, introgression, and selection. Bay et al. find evidence that some alleles have repeatedly introgressed from rainbow trout into cutthroat trout in independent populations. Their results suggest that selection has played an important role in this introgression, and highlight the usefulness of species introductions for understanding the predictability of evolution. Below, get a behind the scenes look at this work from author Rachael Bay.

West slope cutthroat trout. Photo by Ernest Keeley.

What led to your interest in this topic / what was the motivation for this study? 
This study combined two of my primary research interests. The first is: How do humans alter the evolutionary trajectories of species? By introducing rainbow trout, we have provided access to an extended gene pool for native cutthroat trout species. Previous studies have shown that hybrids have lower fitness, but with hybridization and recombination continuing over decades we can investigate whether particular rainbow trout alleles might be adaptive in westslope cutthroat trout. This study also speaks to the predictability of evolution. The stocking of rainbow trout has resulted in a highly replicated evolutionary experiment. Do we find the same alleles repeatedly under positive selection in independent watersheds?

What difficulties did you run into along the way? 
One of the main difficulties was trying to understand the null expectation. How much introgression should we expect between the two species and what fraction of that introgression is a result of selection? This depends on not only the strength of selection, but also on other demographic factors like population size, and stocking history. Ultimately, we decided to use simulations in order to understand the level of selection necessary to produce the patterns of introgression we were seeing in hybrid populations.

What is the biggest or most surprising finding from this study? 
We found that across multiple independent locations, the same rainbow trout alleles rose to high frequency in hybrid populations, suggesting they were under positive selection. This is somewhat surprising because previous studies have suggested that hybrids have reduced fitness and have found broad signals of purifying selection against rainbow trout alleles. However, hybridization and backcrossing has been occurring for many generations, allowing plenty of time for recombination and allowing different parts of the rainbow trout genome to segregate more independently. So despite the fact that hybrids have lower fitness, there seem to be a few regions of the rainbow trout genome that may be advantageous to westslope cutthroat trout.

Moving forward, what are the next steps for this research?
While our results suggest that some rainbow trout alleles provide an adaptive advantage we still have yet to identify the selective force. Is there some component of the abiotic environment to which these alleles are better adapted? Do these alleles confer higher reproductive success or fecundity? Rainbow trout have been successfully introduced to many different environments across North America – do alleles at high frequency in hybrid populations also explain the invasion success of rainbow trout?

What would your message be for students about to start their first research projects in this topic? 
I think it’s really important to choose your system carefully. We didn’t start out thinking about this as a project on trout, we started thinking about human-induced evolution and repeatability. It took a long time and a lot of thought to realize that a broadly introduced species was the perfect natural experiment for the questions we had.

What have you learned about science over the course of this project?
One of the cool things about this project is that it is a demonstration of how science evolves as technology evolves. Through a collaboration with Rick Taylor, we were able to learn something new from samples that had been sitting in a freezer for many years. Previous researchers had used these samples to analyze rates of hybridization across British Columbia and Alberta, but the increasing ease of high-throughput sequencing allowed us to take a deeper dive and look at genome-wide signals of introgression. So you never know how experiments you are doing now will contribute to knowledge in the future!

Describe the significance of this research for the general scientific community in one sentence.
Some genes from introduced rainbow trout can confer an adaptive advantage in native cutthroat trout species.

Describe the significance of this research for your scientific community in one sentence.
Rainbow trout alleles show consistently high levels of introgression into the westslope cutthroat trout genome across multiple independent watersheds.

Read the full article:
Bay RA, Taylor EB, Schluter D. Parallel introgression and selection on introduced alleles in a native species. Mol Ecol. 2019;28:2802-2813.