Sex-Dependent Carry-Over Effects Between Physiological State and Reproduction in a Passerine Species

Abstract

Carry-over effects (COEs) occur when an event in a life stage of an individual is affected by the experience, physiological state or reproduction of a previous life stage. COEs are insufficiently explored with regard to the connections between physiological state and reproduction in animals with seasonal iteroparity and short lifespans. We investigated within-individual temporal changes in haematocrit (an indicator of oxygen-carrying capacity and energetic demand) and heterophil granulocyte-to-lymphocyte (H/L) ratio (indicator of stress levels and health state) within and between breeding seasons, and COEs between haematocrit, H/L ratio, and reproduction (breeding onset, clutch size, brood size and the number of prefledglings) in a short-lived passerine, the collared flycatcher (Ficedula albicollis). Haematocrit varied across years and showed moderate repeatability overall, with higher repeatability observed in females. In males, haematocrit declined between the courtship and the nestling-rearing period. Lower haematocrit during nestling rearing was associated with higher brood size in males, suggesting a trade-off between self-maintenance and parental effort. While H/L ratio did not fluctuate across years, in females, increased reproductive effort in the previous year correlated with higher H/L ratios in the subsequent year, indicating physiological costs of reproduction. Additionally, females with higher H/L ratio during nestling-rearing had lower fledging success in the following year, suggesting long-term fitness consequences of stress. Our findings highlight that COEs between physiology and reproduction in the short-lived collared flycatcher manifest differently in the two sexes, likely due to distinct reproductive roles and energetic constraints.

Keywords: H/L ratio; breeding success; collared flycatcher; haematocrit; reproductive role; stress.

FIGURE 1

Decrease of haematocrit in male collared flycatchers between courtship and nestling‐rearing period. The dots show the haematocrit values, and the lines connect the values of the same individuals.

FIGURE 2

Relationships (with the 95% confidence intervals [dotted lines]) between current‐year reproduction and physiology during the nestling‐rearing period of collared flycatchers. (a) In males, the relationship between haematocrit during the nestling‐rearing period and regression residuals of brood size on median laying date; and (b) in females, the relationship between H/L ratio during the nestling‐rearing period and median laying date. The continuous red lines show the values predicted by the models.

FIGURE 3

Carry‐over effects in relation to H/L ratio during the nestling‐rearing period in female collared flycatchers. Relationships (with the 95% confidence intervals [dotted lines]) between (a) regression residual of previous‐year clutch size on median laying date and current H/L ratio. (b) current H/L ratio and the regression residuals of the next‐year number of fledglings on median laying date. The continuous red lines show the predicted values predicted by the models.

FIGURE 4

Summary of the associations between physiological states of different life phases, and relationships between reproduction and physiological state during nestling rearing in (a) female and (b) male collared flycatchers (Solid red arrow: positive relationship; dotted blue arrow: negative relationship; outlined red arrow: repeatability; dashed green arrow: decrease; thin solid grey arrow: no relationship).