Trade-offs between personal immunity and reproduction in the burying beetle, Nicrophorus vespilloides

Abstract

We know that parental investment and immune investment are costly processes, but it is unclear which trait will be prioritized when both may be required. Here, we address this question using the burying beetle Nicrophorus vespilloides, carrion breeders that exhibit biparental care of young. Our results show that immunosuppression occurs during provision of parental care. We measured phenoloxidase (PO) on Days 1-8 of the breeding bout and results show a clear decrease in PO immediately from presentation of the breeding resource onward. Having established baseline immune investment during breeding we then manipulated immune investment at different times by applying a wounding challenge. Beetles were wounded prior to and during the parental care period and reproductive investment quantified. Different effects on reproductive output occur depending on the timing of wounding. Challenging the immune system with wounding prior to breeding does not affect reproductive output and subsequent lifetime reproductive success (LRS). LRS is also unaffected by applying an immune elicitor prior to breeding, though different arms of the immune system are up/downregulated, perhaps indicating a trade-off between cellular and humoral immunity. In contrast, wounding during breeding reduces reproductive output and to the greatest extent if the challenge is applied early in the breeding bout. Despite being immunosuppressed, breeding beetles can still respond to wounding by increasing PO, albeit not to prebreeding levels. This upregulation of PO during breeding may affect parental investment, resulting in a reduction in reproductive output. The potential role of juvenile hormone in controlling this trade-off is discussed.

Pathogen and immune dynamics during maturation are explained by Bateman's Principle

“…a), but certainly not the complete suppression was seen in Manduca sexta larvae (Eleftherianos et al ., ). Indeed, injection of an inactive immune elicitor has also been shown to suppress PO activity in this species of beetle partially, potentially as a result of a trade‐off with concomitantly upregulated AMP activity, so this suppression is unsurprising (Reavey et al ., ). PO activity was shown to recover more quickly in mature beetles, contradicting our prediction that immature beetles would have heightened immune responses.…”

“…As the first 24 h of the breeding bout are highly costly (Boncoraglio & Kilner, ), there must still be a trade‐off during this time between reproduction and immunity. The downregulation of PO enzyme activity which has been shown to occur during breeding bouts in N. vespilloides females (Reavey et al ., ) is evidence of a trade‐off between breeding and immunity. However, this was shown to be short‐term, just like the costs of breeding, with PO activity returning to constitutive levels by the end of the breeding bout.…”

Aging in personal and social immunity: do immune traits senesce at the same rate?

“…Hemolymph could only be sampled from each beetle once, as wounding alone will trigger an immune response (Reavey et al. ). Therefore, separate individuals in discrete groups ( n = 18) were used for each age class (total sample size = 162 beetles).…”

“…) and that maintaining personal immunity is also costly (Reavey et al. ). Burying beetles therefore provide us with a system that allows us to easily consider both personal and social immune investment across lifespan.…”

“…We hypothesize that personal immune function will decline with age and that it will be suppressed in breeding beetles (Reavey et al. ), but perhaps this suppression will be exacerbated with old age when residual reproductive value declines. If social immunity follows a pattern of parental investment, we might expect an initial increase, but lower levels of lytic activity in later life.…”