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The standard evolutionary theory of ageing predicts a negative relationship (trade-off) between fecundity and longevity. However, this relationship can become positive: (i) under the influence of longevity-enhancing mutations; (ii) when individuals have unequal resources; and (iii) in eusocial insects, in which reproductive queens outlive less- or non-reproductive workers. Developmental diet is likely to be central to determining trade-offs as it affects key fitness traits such as adult body size, but its exact role remains uncertain. For example, inDrosophila melanogasterfruit flies, changes in adult diet can affect fecundity, longevity, and gene expression throughout life, but it is unknown how changes in developmental (larval) diet affect fecundity-longevity relationships or gene expression in adults. UsingD. melanogaster, we therefore tested the hypothesis that variation in developmental diet alters the directionality of fecundity-longevity relationships in adults, and characterised associated gene expression changes. We rearedD. melanogasterlarvae on low (20%), medium (100%), and high (120%) SYA (Sugar Yeast Agar) diets, and transferred adult females developing from these larvae to a common (110% SYA) adult diet. We measured life-time fertility (realised fecundity) and longevity of individual adult females and, using mRNA-seq, profiled gene expression changes across two time-points. Adult females raised on the different larval diets exhibited fecundity-longevity relationships that were significantly different in directionality, i.e., varied from positive to negative, despite minimal differences in mean life-time fertility or longevity. Treatments also differed in age-related gene expression, including expression of genes known to be associated with ageing. Hence, this study shows that the sign of fecundity-longevity relationships in adult insects can be altered and even reversed by variation in larval diet quality. Furthermore, larval diet quality may be a key mechanistic factor underpinning positive fecundity-longevity relationships observed in species such as eusocial insects.

Capsule: Early male arrival on the breeding grounds results in early pairing but not early nesting in chiffchaffs, and chiffchaffs can nest, fail and re-nest before willow warblers begin nesting. Aims: To quantify the consequences of timing of arrival for the subsequent timing of pairing, nesting and re34 nesting of a short-distance (chiffchaff, Phylloscopus collybita) and long-distance (willow warbler, Phylloscopus trochilus) migratory species. Methods: The arrival dates of 118 chiffchaffs, and 20 willow warblers were measured from March to June over 10 weeks in Foxley Wood nature reserve, Norfolk. Colour-ringing of 56 chiffchaffs (55 males, 1 female) and 11 willow warblers (10 males, 1 female) was used to relate individual arrival dates to timing of male pairing, clutch initiation and re-nesting. Results: Male chiffchaffs started to arrive in early March and increased rapidly in number until early April, while male willow warbler arrival began in early April. Early49 arriving male chiffchaffs paired earlier than later-arriving individuals, but timing of clutch initiation was unrelated to male arrival dates. Early nesting by chiffchaffs allowed replacement clutches following nest loss, the earliest of which occurred 12 days after the first willow warbler male had paired. Conclusions: Although early-arrival in male chiffchaffs does not translate into earlier-nesting, timing of nesting in chiffchaffs was sufficiently early to allow time for replacement clutches following nest loss. The later arrival of willow warblers is likely to mean fewer opportunities for replacement clutches following nest loss. This difference in breeding phenology could therefore contribute to differences in productivity between the species,especially if nest failure rates are high.

Eusocial insect queens have been suggested to be counter-examples to the standard evolutionary theory of ageing through lacking costs of reproduction. Using the bumblebee (Bombus terrestris), we tested this hypothesis experimentally against the alternative that costs of reproduction exist in eusocial insect queens, but are latent, resulting in the positive fecundity-longevity relationship typically found in unmanipulated queens. We experimentally increased queens’ costs of reproduction by removing their eggs, which causes queens to increase their egg-laying rate. Treatment queens had significantly reduced longevity relative to control queens whose egg-laying rate was not increased. In addition, treatment and control queens differed in age-related gene expression based on mRNA-seq in both their overall expression profiles and the expression of ageing-related genes. Remarkably, this occurred principally with respect to relative age, not chronological age. These results provide the first simultaneously phenotypic and transcriptomic experimental evidence of costs of reproduction in queens of eusocial insects and suggest how the genetic pathways underpinning ageing might become remodelled during eusocial evolution.