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Causes and consequences of senescence in wild insects

Periodic Reporting for period 1 - CONSENT (Causes and consequences of senescence in wild insects)

Reporting period: 2018-09-01 to 2020-08-31

Senescence (age related decline in biological performance and increased mortality risk) is ubiquitous in natural populations including humans and short-lived invertebrates, but ageing mechanisms remain poorly understood in nature. The main reason for this is because candidate mechanisms are predominately studied in laboratory systems that do not reflect natural populations.
This project aims to address three major issues that currently limit progress in ageing research:
1. Laboratory model systems are studied in conditions that involve abundant food, no predators and no disease. Consequently, the natural environmental conditions that shaped the evolution of life-history traits are lacking, which dramatically affects the phenotypic expression of ageing and its fitness consequences. There is a pressing need for model systems that can be studied in both lab and field.
2. It is unclear to what extent life-history trade-offs reflect genetic correlations, despite the fact that the heritability of such trade-offs is a prerequisite for natural selection to act directly on them. Existing studies on this subject are ambiguous and do not include insects, the most important group for studying ageing in the lab.
3. Telomere shortening is a promising candidate biomarker of ageing in vertebrates including humans. However, the causes of in vivo telomere shortening remain elusive, which is in part due to telomere attrition being a slow proccess taking decades in humans.

I will study ageing and its underlying mechanism in field crickets both in the lab and in the wild. The project takes advantage of the fact that insects have very short lifespans making it possible to study ageing and the candidate underpinning mechanisms within a relavite short timespan of weeks. The main research objectives are to investigate whether ageing is the result from life-history trade-offs and the extent to which such trade-offs reflect genetic constraints, or environmental effects. I will in detail investigate whether telomere attrition underpins the ageing phenotype of field crickets.
During the first half year of my fellowship I collaborated intensely with Tregenza and his group to analyse all the life-history data the WildCrickets project amassed since 2006 to study my research objectives. The data analyses required advanced statistical approaches and I used my expertise in this context to deliver such analyses and also to transfer these statistical skills to Tregenza and his group. Firstly, I have conducted demographic and individual based analyses of senescence which led to a 2nd author publication in Evolution [1] boasting one of the first detailed longitudinal studies of senescence in a wild insect. Secondly, I used novel threshold modelling techniques that I learned during the fellowship to uncover life-history trade-offs and their impact on senescence to overcome one of the greater challenges in studying longitudinal quadratic patterns, typical of most life-history traits. These analyses led to the discovery that trade-offs appear to be of relative minor importance in shaping the life-history of the field cricket. This work resulted in another 2nd author paper in Evolution [2]. Thirdly, using Tregenza’s expertise on sexual selection theory we studied the impact of sex ratio on senescence, resulting in a third 2nd author paper on senescence in the Proceedings of the Royal Society B [3] and a fourth 3rd author paper on sex differences in senescence in Animal Behaviour [4], both papers relying on threshold modelling. Research objectives 1 & 2 were very successful in that they resulted in a larger number of original research papers than we anticipated. At the same time, we also planned to investigate the additive genetic basis of life-history trade-offs, and I received extensive training in quantitative genetic techniques from Prof Alastair Wilson, and this collaboration and the associated research is ongoing.
The telomere project (research objective 3) involved initial validation and optimisation of the TRF lab assay protocol to measure telomere length in the field cricket, which has not been done previously. I studied the effects of growth acceleration on telomere length by letting nymphs grow from the size of hatchlings to the size of adults at differing temperature conditions, hence making use of the fact that environmental temperature can be used as a simple tool to manipulate the growth rate of ectothermic species. The temperature treatment successfully manipulated the growth rate of nymphs, but I unexpectedly found that this treatment had no discernible effect on telomere length. Through detailed subsequent quantitative genetic analyses it emerged that telomere length is highly heritable indicating that telomere length is determined by additive genetic- rather than environmental effects. A first-author manuscript on these findings is currently under review at Molecular Ecology and if accepted, will feature in a special issue on “Telomeres in Ecology and Evolution”. A pre-print is available on the bioRxiv [5].

1. Rodríguez-Muñoz R, Boonekamp JJ, Liu XP, Skicko I, Pedersen SH, Fisher DN, Hopwood P, 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)
2. Rodríguez-Muñoz R, Boonekamp JJ, Liu XP, Skicko I, Fisher DN, Hopwood P, Tregenza T. 2019 Testing the effect of early‐life reproductive effort on age‐related decline in a wild insect. Evolution 73, 317–328. (doi:10.1111/evo.13679)
3. Rodríguez-Muñoz R, Boonekamp JJ, Fisher D, Hopwood P, Tregenza T. 2019 Slower senescence in a wild insect population in years with a more female-biased sex ratio. Proceedings of the Royal Society B: Biological Sciences 286, 20190286. (doi:10.1098/rspb.2019.0286)
4. Makai G, Rodríguez-Muñoz R, Boonekamp JJ, Hopwood P, Tregenza T. 2020 Males and females differ in how their behaviour changes with age in wild crickets. Anim Behav 164, 1–8. (doi:10.1016/j.anbehav.2020.03.011)
5. Boonekamp J, Rodríguez-Muñoz R, Hopwood P, Zuidersma E, Mulder E, Wilson A, Verhulst S, Tregenza T. 2020 Telomere length is highly heritable and independent of growth rate manipulated by temperature in field crickets. Biorxiv , 2020.05.29.123216. (doi:10.1101/2020.05.29.123216)
One key implication of my work on telomeres is that it revealed that telomere length is highly heritable. In fact the heritability is so high that it means that all of the among individual variation is due to additive genetic effects. Recent studies of colleagues working on a range of different study species suggest that the high heritability may be a general phenomenon as their research is generally in agreement with the findings of my telomere studies. The high heritability may shift our thinking regarding the suitability of telomere length as an informative biomarker of life-style and ageing, because it implies that telomere length variation is genetic of origin rather than that it is caused by life-style or other environmental effects. On the other hand the fact that telomere length is both heritable and predictive of lifespan underlines a hitherto underappreciated role of telomeres as an innate somatic component of fitness.