Interview with the author: Ecological gradients drive insect wing loss and speciation: The role of the alpine treeline

Many insects have lost their wings at high altitude, and this might have contributed to their diversification. In their recent paper, Graham A. McCulloch and colleagues study loss of wings in stone flies from New Zealand and found that the alpine tree line, rather than altitude alone better explains the ecotypic distribution of these morphs across geography. Their system paves the way for powerful studies of convergence and adaptation and how, like in other systems, loss of a trait, might be intrinsically related to many cases of deterministic evolution in nature. Below, we learn about their journey in discovering some of the causes of diversification of alpine insects and their assemblages.

Sampling wing-reduced stoneflies in the alpine stream habitats of southern New Zealand. Photo by Graham McCulloch

What led to your interest in this topic / what was the motivation for this study? 
An astonishingly large proportion (20%) of New Zealand’s stonefly species (freshwater insects) have reduced wings as adults, with most of these low-dispersal lineages found in alpine environments. Our research group is interested in the ecological drivers and genomic basis of this fascinating pattern: how and why do insect wings become reduced/lost, and what are the consequences of this? The Zelandoperla fenestrata complex in particular is an outstanding system for studying these questions, as this widespread polymorphic stonefly has full-winged populations at low altitudes, but vestigial-winged populations up in the mountains. When we started looking within individual streams, we were amazed to find strikingly clear altitudinal clines within this ‘species’, where wings become dramatically smaller as we move a few hundred metres up a mountainside. This was an exciting finding, so understanding the ecological and genomic basis of these clines became the focus of our research.

What difficulties did you run into along the way?
Our study involved working in rugged mountain landscapes, which can be both exciting and spectacular – but also carries challenges. You need to be fit, and to persist in sometimes uncomfortable conditions. It also can be notoriously difficult to find adults of these stoneflies in the wild, even in the right season, so it was a big logistical breakthrough to be able to successfully rear large nymphs to adulthood in the lab. This breakthrough really allowed us to get a good handle on the system morphologically.

What is the biggest or most surprising finding from this study?
There were several unexpected and exciting discoveries from this project: (i) We were particularly excited to find a tight association between wing-reduction and the alpine treeline, both at a fine scale (within our transects), and at a broader scale (using distributional analyses). These results suggest that harsh conditions above the alpine treeline (most likely high winds) are a major driver of insect wing loss. (ii) The genome-wide divergence between the full-winged and vestigial-winged ecotypes within each stream was particularly surprising, as these ecotypes have overlapping distributions (and interbreed in the wild). Likewise, the genome-wide divergence between the two independent vestigial-winged alpine populations, from streams less than 3km apart, was astonishing given the small distance involved.

image
The alpine treeline governs the distribution of full‐winged versus vestigial‐winged stoneflies. (a) Jitter plot illustrating the bimodal wing‐length data associated with distinct Zelandoperla fenestrata ecotypes collected from two parallel streams (Lug Creek, Six Mile Creek) on the Rock and Pillar Range, South Island, New Zealand. Inset: dorsal view of full‐winged (above) and vestigial‐winged (below) Z. fenestrata ecotypes (body length 15 mm). (b) The alpine treeline in Lug Creek, where riparian tree cover rapidly gives way to tussock grassland. (c) Altitudinal clines in relative proportions of wing ecotypes in Lug Creek (dashed line) and Six Mile Creek (solid line). Vertical green lines indicate the altitude of the alpine treeline for each stream (Lug Creek = dashed line, Six Mile Creek = solid line)

Moving forward, what are the next steps for this research?
We plan to examine additional ecotypic clines in this species across the lower South Island. This next step will allow us to assess whether the genome-wide differentiation we observe between ecotypes in the Rock and Pillar range is found in other regions. By genetically characterising geographically (and phylogenetically) independent clines we can then test for independent wing loss events (associated with the alpine treeline) more broadly. We are also in the process of using genomic (GWAS) and transcriptomic approaches to identify the key genes underpinning wing-reduction in Z. fenestrata (and potentially other alpine stonefly species). We are really keen to find out whether the wing reduction events in different streams and mountains involve the same genes dispersed by winged populations (e.g. transporter hypothesis), or whether they are completely independent.

What would your message be for students about to start their first research project in this topic?
Discovering this fascinating research system took time – including quite a bit of ground-work exploring out in the field, background research to understand the species complex, including discussions with entomologists, taxonomists, looking at museum collections, and then putting a team together with the skills to get the work done. So it didn’t happen overnight, and it took time to set the stage and to know for sure that we’d found a good system. But it really started from curiosity about evolution, as well as our ongoing interest in New Zealand’s landscapes and natural history. So our most important advice is to follow your curiosity, and keep exploring the natural world.

What have you learned about science over the course of this project?
We have learned that there are still plenty of exciting discoveries yet to be made about nature, evolution and ecology – and that the more we discover, the more new questions emerge. It might take five or ten years to really understand a system to the extent that you can begin to answer the most exciting questions. We certainly expect to keep working on this project for many years to come.

Describe the significance of this research for the general scientific community in one sentence.
We have discovered what we believe to be a ‘textbook example’ of speciation in action – one that makes evolutionary biology easier to teach and understand.

Describe the significance of this research for your scientific community in one sentence.
This story brings together ecological and genomic tools to reveal clear-cut cases of parallel ecological speciation over surprisingly small spatial scales.

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