Comparing individual and population measures of senescence across 10 years in a wild insect population

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.

Telomere length is highly heritable and independent of growth rate manipulated by temperature in field crickets

“…It is reasonable to hypothesize the same is true in insects, although this remains to be verified. We have demonstrated the existence of both actuarial and phenotypic senescence in the few weeks of the adult phase of the life cycle of our wild field crickets (Rodríguez-Muñoz et al 2019b), and similar observations exist in a number of insects (Tatar et al 1993;Bonduriansky & Brassil 2002;Hunt et al 2004;Sherratt et al 2011). Furthermore, G. campestris spend >70% of their life as growing nymphs, and from a theoretical perspective this extensive period of growth / cell divisions should not restrict the potential for nymphs to show substantial telomere attrition.…”

Slower senescence in a wild insect population in years with a more female-biased sex ratio

“…We are still processing the video from 2014 and 2017, and in 2006 we did not record temperature data so those years are not used in the present analysis. The meadow is managed in a similar way every year (for details of management and our monitoring regime, see [12,13]). By mid to late April, usually before the adults start to emerge, we install up to 133 infrared day/night cameras that record the activity around each burrow entrance continuously.…”

“…Previous analyses examined potential phenotypic senescence across a range of male traits [13], and identified male calling activity as the trait with the most robust evidence for senescence. In our study population, calling activity increases with age until it reaches a peak and declines subsequently [13]. We quantified calling activity for each male by recording whether he was calling or not over the first 10 min of every hour he was under observation.…”

“…Over 10 years, we have closely monitored the survival and behaviour of a natural population of field crickets, Gryllus campestris in a meadow in northern Spain [12]. Each year we tag every individual in the population and by monitoring them for 24 h a day, using a network of video cameras, we have minute by minute measurements of phenotypic trait expression in both males and females and very precise demographic data [13].…”

Distinguishing within- from between-individual effects: How to use the within-individual centering method for quadratic patterns

“…In the case of age patterns, the among-individual effect may be generated by both selective appearance and disappearance effects (van de Pol and Verhulst 2006), making estimation of the among-individual effect more complicated. In addition, several studies strongly suggest moving away from polynomial models in favour of threshold models when studying aging patterns (Berman et al 2009; Froy et al 2017; Murgatroyd et al 2018; Rodríguez-Muñoz et al 2019). In this context, an interesting alternative method closely related to the within-individual centering is the use of age at first and last reproduction as fixed covariates (van de Pol and Verhulst 2006).…”