Seasonal reproductive tactics: annual timing and the capital-to-income breeder continuum

Abstract

Tactics of resource use for reproduction are an important feature of life-history strategies. A distinction is made between 'capital' breeders, which finance reproduction using stored energy, and 'income' breeders, which pay for reproduction using concurrent energy intake. In reality, vertebrates use a continuum of capital-to-income tactics, and, for many species, the allocation of capital towards reproduction is a plastic trait. Here, we review how trophic interactions and the timing of life-history events are influenced by tactics of resource use in birds and mammals. We first examine how plasticity in the allocation of capital towards reproduction is linked to phenological flexibility via interactions between endocrine/neuroendocrine control systems and the sensory circuits that detect changes in endogenous state, and environmental cues. We then describe the ecological drivers of reproductive timing in species that vary in the degree to which they finance reproduction using capital. Capital can be used either as a mechanism to facilitate temporal synchrony between energy supply and demand or as a means of lessening the need for synchrony. Within many species, an individual's ability to cope with environmental change may be more tightly linked to plasticity in resource allocation than to absolute position on the capital-to-income breeder continuum.This article is part of the themed issue 'Wild clocks: integrating chronobiology and ecology to understand timekeeping in free-living animals'.

Keywords: capital breeding; income breeding; life-history; phenology; resource allocation.

Figure 1.

Current view of the mechanisms responsible for activation and modulation of the reproductive axis in birds and mammals. Changes in photoperiod or the circannual clock activate the hypothalamus-pituitary-gonadal axis via the EYA3-TSH-Dio-T3 pathway. In mammals, this occurs via the melatonin signal whereas deep brain photoreceptors (DBP) also play a role in birds. Metabolic state influences timing via effects of glucocorticoids (GCs), leptin and ghrelin on the RF-amides kisspeptin (KISS), and GnIH; reproductive inhibition in response to these signals is also probably occurring at the level of the gonads. Dashed black arrows from T3 indicate multiple pathways that may vary across taxa. The KISS signalling pathway, for example, appears to be non-functional in birds. Ambient temperature is also hypothesized to influence timing via transient receptor potential (TRP) thermoreceptors. Solid coloured arrows indicate effects of physical cues (photoperiod—orange; temperature—red) or metabolic cues (blue) on hormones/neurons that in turn influence the reproductive axis (via connections shown in dashed lines). GnRH-II (not shown) also appears to have a neuromodulatory role in affecting feeding and reproduction.

Figure 2.

Increase of heart rate from winter to summer and modulation by food availability in adult female red deer (n = 15). Plotted are hourly means of heart rate of individuals with unrestricted (blue) or restricted access to food (red, for methodological details see [61]). Shaded belts indicate 95% confidence limits (CI) of smooths fitted to seasonal changes by general additive mixed modelling (R-package ‘mcgv’), including a cosinor term accounting for within-day variation and individual cosinor fits as random factor accounting for repeated measurements. To correct for temporal correlation detected in the residual error term of the model, we included an auto-regressive correlation structure (‘corARMA’ from R-package nlme). Horizontal bars indicate 95% CI of the timing of troughs and peaks, vertical bars 95% CI of trough and peak heart rates. CIs were determined from respective distributions produced by simulating 10 000 replicates of model coefficient vectors from the posterior using ‘mvrnorm’ from R-package MASS. Data shown are from [61], with additional analyses to identify temporal differences between groups in the seasonal peaks and troughs of heart rates.

Figure 3.

Conceptual model illustrating how individual optimization influences the trade-off between reproductive timing and use of capital in a mixed-strategy breeder. (a) Optimal timing is earlier for an animal with large body stores (black line) versus low body stores (blue line); individuals with low body stores delay breeding in order to take advantage of the seasonal peak in resource availability; the percentage of energy allocated towards reproduction that can come from income is represented by the dashed red line (i.e. % income increases with the seasonal increase in resource availability and then begins to fall after the resource peak). Breeding earlier requires a greater investment of capital (grey shaded area above dashed red line) relative to income (non-shaded area below dashed red line) for successful reproduction. (b) Under warming conditions and earlier springs, animals respond plastically to their environment and advance the onset of the breeding season; stabilizing selection maintains an appropriate plastic response and optimal timing for a given physiological condition. (c) Under continued warming, the timing of reproduction fails to advance sufficiently to maintain synchrony with phenological shifts occurring at lower trophic levels and mismatches occur such that selection acts on the mechanisms that control timing and/or the sensitivity of these mechanisms to environmental cues.

Figure 4.

Recruitment success of red squirrels has varied substantially over the past 20 years due to high annual variation in the production of cones by white spruce (a). Timing of reproduction in food-hoarding red squirrels is dictated by the size of the previous year's spruce cone crop (b), which determines the amount of capital available for reproduction. Females that breed earlier are more reliant on capital, both within and across years (c). In panel (c), each pair of points connected by a solid line represents one study year; early- and late-breeding squirrels reached mid-lactation (35 days postpartum) prior to, or after, the yearly median mid-lactation date, respectively. Panels (a) and (b) from [82], panel (c) from [23].