Summary from the authors: Standing genomic variation within coding and regulatory regions contributes to the adaptive capacity to climate in a foundation tree species

Photos clockwise: a fully mature marri tree (Corymbia calophylla; by R. Mazanec), the characteristic large gumnut (by R. Davis), and the flowers (by R. Davis).

Marri, an economically and ecologically important tree in the southwest Australian floristic region, is under pressure from the effects of climate change, notably heatwaves and droughts. In this study we focus on understanding how this species is adapted to climate, providing information to develop evidence-based forest management policy, which aims to improve the tree’s persistence in a future climate. We used genomic techniques to explore genetic variation along climate gradients that are indicative of adaptation. We found adaptive genomic variants within and immediately up stream of functional genes that play key roles under temperature and water stress. Genomic variants within genes can lead to changes to the function of the protein themselves, providing opportunities for selection, while genomic variants upstream of genes may alter regulation, producing a varying amount of proteins. Both of these are important ways in which organisms are able to adapt to different climatic conditions. The amount of adaptive genetic variation within and around genes suggests the species can persist under the pressures and pulses of climate change with the help of evidence-based, proactive forest management.

Ahrens CW, Byrne M, Rymer PD. Standing genomic variation within coding and regulatory regions contributes to the adaptive capacity to climate in a foundation tree species. Mol Ecol. 2019;28:2502–2516. https://doi.org/10.1111/mec.15092

Interview with the author: Sex allocation plasticity on a transcriptome scale: Socially sensitive gene expression in a simultaneous hermaphrodite

Morphological evidence has long supported that simultaneous hermaphrodites invest more into the male sexual function at larger group sizes. In their recent work, Steven Ramm and colleagues use transcriptomic data link this morphological response to gene expression. Learn more about their study below, and in the full paper.

Ramm SA, Lengerer B, Arbore R, et al. Sex allocation plasticity on a transcriptome scale: Socially sensitive gene expression in a simultaneous hermaphrodite. Mol Ecol. 2019;28:2321–2341. https://doi.org/10.1111/ mec.15077

Sex allocation plasticity in Macrostomum lignano from a morphological perspective. The investment into testes (Te, blue) and ovaries (Ov, orange) can be readily quantified in these transparent flatworms (as illustrated in the inset) and used to derive a proxy for sex allocation (as testis area/[testis area + ovary area]). We confirmed that sex allocation varies significantly with the group size treatment (see main text for details). This represents a by now well‐established phenotypically plastic response that we here investigate further from a transcriptional landscape perspective 

What led to your interest in this topic / what was the motivation for this study? 
We’ve long since known about the ability of many simultaneous hermaphrodites to adjust their sex allocation at a morphological level, fine tuning their investment into their male and female sex functions according to cues in their social environment so as to maximise their total fitness returns. More specifically, at larger group sizes, individuals have to compete more to gain fertilisations and it therefore pays to shift investment from their female to their male sex function. The exciting prospect with this study was to be able to link this morphological response to the underlying plasticity in gene expression in organs such as the testis and ovary.

What difficulties did you run into along the way? 
One difficulty in switching from a morphological to a transcriptomic level of analysis was simply the sheer amount of data that we generated. We were measuring gene expression in tens of thousands of transcripts and found thousands of differentially expressed candidates that differed in expression according to the social environment, making it initially difficult to decide how best to focus our follow-up studies of the transcriptomic data.

What is the biggest or most surprising finding from this study? 
For me, one of the biggest surprises was that such a large proportion of the M. lignano genome is differentially regulated in its expression according to the social environment. There are different ways we measured that, but at least 10% of the transcriptome showed evidence for variable expression depending on something as simple as the number of other flatworms they regularly encountered. That’s of course both a blessing and a curse, since we’ve still got a big task ahead figuring out the functional roles of all those genes, and in particular the key gene expression changes within the subset of differentially expressed transcripts that really drive the plasticity.

Moving forward, what are the next steps for this research? 
One thing we’ve already been following up on in some detail is that alongside many transcripts which we expected to be plastically expressed in the testis and ovary (since these are the key organs for sex allocation), we found an additional large class of genes that were also highly plastic in their expression and are predominately or exclusively expressed in the tail of the flatworms. We’ve now found that many of these are expressed in the prostate gland cells responsible for seminal fluid production, another key component of male allocation, opening up the possibility of studying their functional and adaptive significance for sperm competition and sexual conflict.  

What would your message be for students about to start their first research projects in this topic? 
Be realistic about what that project can achieve. The ability to measure gene expression on a transcriptome scale has been a huge boon for the field, and opens up many exciting possibilities. But because we can now measure everything at once, there’s always a risk of drowning in data. If, for example, we would now follow up on all the plastically expressed genes we found in our study, that could easily fill several PhD projects. Clear questions and good experimental design become even more important as technology advances, not less.

What have you learned about science over the course of this project? 
The importance of collaboration. I’ve benefited from working with a great team of people spread across four different countries, which allowed us to combine several different techniques (morphological assays, RNA-Seq, in situ hybridisation, RNAi) in a single study. 

Describe the significance of this research for the general scientific community in one sentence.
Our project has begun to show how the dynamic allocation of resources to producing either sperm or eggs in hermaphroditic organisms occurs at the underlying level of the genes responsible for spermatogenesis and oogenesis, respectively. 

Describe the significance of this research for your scientific community in one sentence.
I hope our research can move sex allocation research forward on a couple of fronts: primarily, it offers a first – though still far from complete – glimpse into the mechanisms of phenotypic plasticity in simultaneous hermaphrodites; and second, it provides the starting point for deciphering the functions of a vast swathe of genes now implicated as being of adaptive significance for either the male or female sex function.

Summary from the authors: What is responsible for genetic fragmentation? Spatiotemporally explicit model testing can help to reach the answer

An important task of conservation genetics is to determine whether spatial patterns of genetic structure were driven by historical processes of population isolation (e.g. the presence of natural barriers to dispersal) or if they are a consequence of human activities (e.g. habitat destruction and fragmentation). Resolving this question is not trivial and has important implications for establishing proper on-ground management practices: Do distinct genetic groups represent evolutionary significant units that deserve to be preserved or, on the contrary, is genetic fragmentation a consequence of anthropogenic habitat destruction and conservation actions should focus on restoring population connectivity? In this study, we used genomic data and a spatiotemporally explicit model-based approach to test these hypotheses in a red listed grasshopper endemic to the Iberian Peninsula. Our demographic analyses indicate that although natural barriers to dispersal (mountains) are the main factors determining spatial patterns of genomic variation in the study species, anthropogenic habitat destruction has also contributed to the genetic fragmentation of its populations. This study emphasizes the potential of model-based approaches to gain insights into the temporal scale at which different processes impact the demography of natural populations of great conservation concern. – María José González Serna, Personal investigador UCLM

Photo courtesy of Piluca Álvarez.

González-Serna, M. J., Cordero, P. J. and Ortego, J. 2019. Spatiotemporally explicit demographic modelling supports a joint effect of historical barriers to dispersal and contemporary landscape composition on structuring genomic variation in a red-listed grasshopper.Molecular Ecology, 28:2155-2172.

Interview with the author: Chromosome polymorphisms track trans‐Atlantic divergence and secondary contact in Atlantic salmon

Populations of salmon in the eastern and western Atlantic ocean diverged more than 600,000 years ago. They survived in isolated refugia during the glacial maxima, and later expanded their ranges. When colonizing northern areas after the retreat of the glaciers, eastern and western populations came back into contact. Lehnert et al. studied the genome-wide consequences of secondary contact, with a particular focus on regions of the genome near chromosome rearrangements. One chromosomal rearrangement shows evidence of European ancestry in North American individuals, suggesting that secondary contact occurred during the colonization of northern part of the species’ range. However, another chromosomal rearrangement showed a contrasting pattern: evidence of a derived North American chromosome fusion. In both rearrangements, the authors find evidence of natural selection, suggesting that chromosomal rearrangements may serve an adaptive role in salmon. Below, we go behind the scenes with Dr. Sarah Lehnert, currently Postdoctoral Fellow at Fisheries and Oceans Canada, to learn more about the findings of the paper and the work that went into this research. You can find the associated paper here: https://onlinelibrary.wiley.com/doi/10.1111/mec.15065

Atlantic salmon (Salmo salar) Gaspe Peninsulsa, Quebec, Canada. October 2017.
Photo credit: Nick Hawkins

What led to your interest in this topic / what was the motivation for this study? 
Atlantic salmon populations across the North Atlantic have been declining in recent decades. Our lab is interested in better characterizing genetic structure and diversity of salmon populations in North America to improve conservation and management. When we started this project, I was interested in identifying genomic regions associated with large-scale differences among individuals across populations. We were particularly interested in identifying genomic variation associated with historical secondary contact (~10,000 years ago) between European and North American Atlantic salmon. These groups diverged >600,000 years ago and mitochondrial evidence suggest contact has occurred but genomic evidence is limited. For our project, we investigated if and how secondary contact has influenced contemporary population structure and considered the implications for salmon management and conservation.

What led to your interest in this topic / what was the motivation for this study? 
Atlantic salmon populations across the North Atlantic have been declining in recent decades. Our lab is interested in better characterizing genetic structure and diversity of salmon populations in North America to improve conservation and management. When we started this project, I was interested in identifying genomic regions associated with large-scale differences among individuals across populations. We were particularly interested in identifying genomic variation associated with historical secondary contact (~10,000 years ago) between European and North American Atlantic salmon. These groups diverged >600,000 years ago and mitochondrial evidence suggest contact has occurred but genomic evidence is limited. For our project, we investigated if and how secondary contact has influenced contemporary population structure and considered the implications for salmon management and conservation.

What difficulties did you run into along the way? 
We first investigated genomic regions that showed large-scale inter-individual variation across North American populations. One difficulty was that many approaches are designed to investigate population level differences rather than individual differences. By using methods that allow the investigation of individual variation in addition to population level differences, this enabled us to resolve karyotypic differences within populations that may have been missed by other analyses. This led us to identify variation in two chromosomal rearrangements (translocation and fusion). The next difficulty was trying to understand why these rearrangements show different geographic structure and different levels of diversity. Through additional analyses and by incorporating European samples, we determined that variation in each chromosomal rearrangement evolved through different mechanisms.

What is the biggest or most surprising finding from this study? 
Our work suggests that Atlantic salmon within rivers in North America have different numbers of chromosomes. This corroborates earlier karyotyping studies in a few rivers, but our study is the first to show genomic evidence of chromosome variation at the continental scale and our work also identifies which chromosomes are responsible for this variation and how this variation came to be. What was most exciting to me was being able to use SNP data to understand the different evolutionary histories of these chromosomal rearrangements. Our study revealed an interesting story as we found that variation in one chromosomal rearrangement was introduced from European salmon coming to North America whereas variation in the other chromosomal rearrangement evolved within North America independently.

Moving forward, what are the next steps for this research?
We found that chromosome variation exists in North American Atlantic salmon and our next step is to further understand why this variation exists. Our study suggested that these regions were under selection and thus we hypothesize that chromosome variation may relate to life history diversity or local adaptation. In other salmonids, chromosomal rearrangements have been associated with important traits such as migration phenotype. The fusion identified in our study has recently been suggested to be associated with precipitation within a single river system. Therefore, we plan to sample a wider range of populations in North America and examine environmental and life history variation associated with karyotype differences at a continental scale

What would your message be for students about to start their first research projects in this topic? 
My advice would be to read new papers but also old papers on your study system. By reading older papers, I learned that some earlier studies had identified karyotype variation within and between Atlantic salmon populations. This was not often discussed in more recent population genetic studies that focused on microsatellites or SNPs. Reading older karyotyping studies on Atlantic salmon in conjunction with new papers (reviews) on chromosomal variation helped me formulate hypotheses and interpret the patterns we were finding in the genome. It can be easy to focus on recent literature, but older work can often help shed a different light on unresolved questions.

What have you learned about science over the course of this project? 
Through this work, I have learned that variation in chromosome structure is prevalent across taxa. Dobzhansky highlighted this as early as the 1930s but the field of genetics moved away from this earlier focus on chromosome level differences. Only recently have we started to appreciate how important chromosomal structure variation may be to adaptation. Within the last decade, chromosomal inversions have been associated with complex phenotypes such as mating tactics in the ruff and migration strategy in species like cod, warblers, and rainbow trout. Although inversions have recently garnered a lot of attention, our study also highlights the importance of variation in chromosomal fusions and translocations, which have not been identified within many animal populations to date.

Describe the significance of this research for the general scientific community in one sentence.
Our research demonstrates variability in chromosomal translocations and fusions within populations of a vertebrate species that may play a role in adaptation and highlights how historical events (glaciations and secondary contact) can influence contemporary diversity.

Describe the significance of this research for your scientific community in one sentence. 
Our work suggests that differences in chromosome number are prevalent in Atlantic salmon populations and this potentially adaptive variation can provide information about different evolutionary events, highlighting the importance of such genetic variation to salmonid populations management.

Summary from the authors: Genomics, environment and balancing selection in behaviourally bimodal populations: The caribou case

Like people, caribou are individuals. Each animal has a different colouration pattern, size, metabolism and other characteristics. And each behaves differently, including in specific environments. But what drives such differences, or diversity, in caribou? Are such mechanisms similar in other animals, including people? And can understanding what gives rise to such diversity help conserve caribou, a threatened species in Canada, which recently became functionally extinct in the Lower 48 US? This study has identified a natural mechanism in caribou that preserves and ensures long-term genetic and behavioural diversity of the species in various habitats across western North America, from Alaska to the Southern Canadian Rockies. This mechanism, called “balancing selection,” has resulted in caribou populations having not only distinctly different genetic traits but also diverse and likely adaptive behaviours, including whether individual animals migrate or not. Balancing selection could ensure that two or more behaviours or characteristics are selected at the same time, by balancing the benefits of one type of behaviour or appearance with the benefits of other types. This research is the first genomic study of caribou and perhaps the first to confirm the gene-driven balancing selection mechanism in a wild species in nature. – Marco Musiani

Cavedon, M., Gubili, C., Heppenheimer, E., vonHoldt, B., Mariani, S., Hebblewhite, M., … Musiani, M. (2019). Genomics, environment and balancing selection in behaviourally bimodal populations: The caribou case. Molecular Ecology, 28(8), 1946–1963.https://doi.org/10.1111/mec.15039