Evolution Highlight: Wild insect senescence

The Evolution Highlights series highlights some of the interesting and varied papers published within the last few years in Evolution. The goal of these Evolution Highlights is to let our readers learn more about how the highlighted study came into existence, and to invite the authors to share stories and tips from the perspective of a recently published author. We welcome nominations and self-nominations for the Evolution Highlights. Find out how to submit a paper here.

"Comparing individual and population measures of senescence across 10 years in a wild insect population"
Rodríguez‐Muñoz, R., Boonekamp, J.J., Liu, X.P., Skicko, I., Haugland Pedersen, S., Fisher, D.N., Hopwood, P. and Tregenza, T. (2019), Comparing individual and population measures of senescence across 10 years in a wild insect population. Evolution, 73: 293-302. doi:10.1111/evo.13674
https://onlinelibrary.wiley.com/doi/full/10.1111/evo.13674

Abstract:
Declines in survival and performance with advancing age (senescence) have been widely documented in natural populations, but whether patterns of senescence across traits reflect a common underlying process of biological ageing remains unclear. Senescence is typically characterized via assessments of the rate of change in mortality with age (actuarial senescence) or the rate of change in phenotypic performance with age (phenotypic senescence). Although both phenomena are considered indicative of underlying declines in somatic integrity, whether actuarial and phenotypic senescence rates are actually correlated has yet to be established. Here we present evidence of both actuarial and phenotypic senescence from a decade‐long longitudinal field study of wild insects. By tagging every individual and using continuous video monitoring with a network of up to 140 video cameras, we were able to record survival and behavioral data on an entire adult population of field crickets. This reveals that both actuarial and phenotypic senescence vary substantially across 10 annual generations. This variation allows us to identify a strong correlation between actuarial and phenotypic measures of senescence. Our study demonstrates age‐related phenotypic declines reflected in population level mortality rates and reveals that observations of senescence in a single year may not be representative of a general pattern.

Evolution Highlight by Tom Tregenza
Centre for Ecology and Conservation, University of Exeter, Pernyn Campus

What gave you the idea for this study?

We’ve been studying a population of crickets in a meadow in Northern Spain for the last 14 years. We call the project ‘WildCrickets’. Rolando Rodríguez-Muñoz and I started the project partly because we started to wonder how relevant all the lab studies that we’d been doing really were, and partly because Rolando was keen to do some work in his native Asturias. We originally focussed on trying to measure natural and sexual selection in the wild and really, just trying to get an idea of what wild insects get up to. Rolando noticed that late in the breeding season those adults that are left become very sluggish, in stark contrast to the zippy little speed-merchants that dash into their burrows at the slightest stimulus early in the season. We started to wonder whether they were experiencing senescence despite only being a few weeks old as adults and a little over a year old in total.

What was the big question you were trying to ask and why was it exciting?

Senescence is an area full of really interesting questions. It’s absolutely central to the life history of all organisms. It’s the product of evolution and not some mysterious inevitability, and it’s really not very well understood at all. Added to that is the fact that we all eventually start to wonder about why we’re getting old and knackered. The thing we wanted to focus on in this study was whether the increase in the probability that an organism will die as it gets older is reflected in declines in its physiological state.

In what ways does this study expand or build on your previous studies?

There are now quite a lot of studies of wild populations that show either that within populations the probability of dying increases with age (actuarial senescence) or that individuals decline in how well they can perform tasks as they get older (phenotypic senescence), but there are very few studies that allow these two metrics to be compared.

From your perspective, what was the most interesting or intriguing aspect of this study?

The thing I was most intrigued by was how much the pattern of ageing varied among years. In some of the ten years we studied, it was very clear, both in terms of actuarial and phenotypic senescence. In other years we couldn’t detect any signal of senescence at all.

Were there any unexpected logistical or technical challenges you had to address?

The whole WildCrickets project has been a series of logistical and technical challenges as we’ve developed the network of 140+ cameras that we use to record as much as we can of the adult lives of every cricket in our meadow. For this project, the biggest challenge turned out to be getting to grips with the horrendous statistics that are needed to quantify patterns of senescence.

Did your work take you to any interesting locations? If so, what were they like?

Our meadow, which is between the mountains and the sea halfway along the north coast of Spain, is a beautiful spot. I always enjoy the juxtaposition between all the technology we have in there; fibre optic convertors and laser surveying equipment and suchlike and the meadow inhabitants making their homes amongst it all.

Tell us something about collecting these data that people might not know or think about.

A great deal of the claims made by CCTV camera and video-capture companies are wilfully exaggerated, or just plain false. We have to try dozens of different bits of kit before finding one that actually works. If you’re planning to video record animals in nature in a situation where cameras are metres (rather than dozens of metres) apart drop us a line and if we can help, we will.

Did you have to learn any new analytical techniques for this study?

Yes! Analysing ageing data is very tricky; you don’t expect linear patterns and the individuals that survive to an old age are not a random sample of the population. We more or less recruited Jelle Boonekamp specifically to assist in the analysis of the data, and input from reviewers proved to be very important as well.

What was your writing process like?

Because we’ve been piling up data since 2006, we often find it difficult to retain a tight enough focus to write a paper that can actually be digested without reading it being a major undertaking. We started off writing a single manuscript which was such hard work that most people we sent it to for comments more or less gave up on trying to understand it. Subsequently we broke the work up into this paper, and two others (“Rodríguez-Muñoz, R. Boonekamp Jelle, J. Fisher, D. Hopwood, P. & Tregenza, T. 2019 Slower senescence in a wild insect population in years with a more female-biased sex ratio. Proc. Roy. Soc. B. 286, 20190286” and “Rodríguez-Muñoz, R. Boonekamp, JJ. Xingping, L. Skicko, I. Fisher, D. Hopwood, P. Tregenza, T. 2018 Testing the effect of early life reproductive effort on age-related decline in a wild insect. Evolution 73, 317-328”). This wasn’t an attempt to ‘sausage slice’ the work to lengthen our CVs, but turned out to be necessary to address specific questions. We write all our WildCrickets papers by dividing up the intro and discussion, the methods, and the results and writing those sections semi-independently with all the main authors bouncing these sections between us until we are happy with the final result.

What was the biggest challenge about writing the manuscript?

An unusual aspect of the review process for this manuscript was that when we submitted the work to Evolution we received some very positive reviews and a classic ‘reviewer 3’ review; the type that you read quickly, then need to go for a walk muttering about what a ******* the reviewer is. We left it a few days, then went through the comments again and ended up deciding they might have a point. Finally we completely reanalysed our data using the approach that the reviewer suggested. This led us to reach a quite different conclusion about what our study was showing, which was rather a humbling experience. We mention this point in the penultimate paragraph of the discussion, by which point hopefully a lot of readers will have already fallen asleep.

Do you have any writing tips for others?

By far my top tip is that the more people you can get to read and comment on your manuscript or grant application before you submit it, the better. I have literally never had a situation where I didn’t learn something from comments from colleagues. Even the ones that when you discuss it, you’re thinking ‘Christ, they don’t get it at all’ are very useful, because if they don’t get it, you can be certain they won’t be the only ones. I am very lucky in being based at Exeter’s Centre for Ecology and Conservation where I have loads of brainiac and super-nice colleagues upon whom I’m totally dependent for this sort of thing (and who would probably have sorted out the grammar in that sentence).

Was this study collaborative with other groups? If so, what was valuable about that experience?

The study was very collaborative in the sense that 17 people, mainly undergraduate students, who are not authors on the study but who spent some weeks helping us watch video are thanked in the acknowledgements, as are 7 colleagues who commented on the manuscript. Also the author list itself includes 3 graduate students Sophie Haugland-Pedersen, Ian Skicko and David Fisher whose own projects were independent of this work, but who took part in collecting data and our Chinese colleague Liu Xingping who was essential to our keeping on top of field monitoring in 2014 when there were several times as many adult crickets in our meadow as we get in a typical year.

What do you think will be the lasting impact of this study?

I hope that this study will help to reinforce the idea that we can study insects in the wild and that we need to do so for years at a time. If we had just studied a single year we would have got a completely misleading picture of what is going on in this system.

What was the most difficult part of this study and / or the most rewarding?

For me the two most rewarding parts of the study were firstly the opportunity to think about the nature of senescence itself and secondly the collaboration with Jelle Boonekamp that it precipitated, and which I am hoping will continue for many years to come.

WildCrickets research group

Data collection