Snakes allocate amino acids acquired during vitellogenesis to offspring: are capital and income breeding consequences of variable foraging success?

Abstract

Reproductive allocation strategies have been historically described as lying on a continuum between capital and income breeding. Capital breeders have been defined as species that allocate stored reserves to reproduction, whereas income breeders have been defined as species that allocate relatively recently‐ingested food resources to reproduction. Snakes are considered capital breeders because they efficiently store large amounts of nutrients and energy, potentially enough to support an entire reproductive bout without feeding. We examined the abilities of five viviparous snake species to allocate income to follicles during vitellogenesis. We fed 15N‐labelled L‐leucine to experimental females of each species during vitellogenesis, whereas control females were fed unlabelled meals. After ovulation, we measured yolk 15N p.p.m. using mass spectrometry. Maternal scale samples taken before labelling were used to estimate endogenous 15N concentrations, which should represent ‘capital’. Scale samples taken at ovulation were used to determine whether snakes assimilated 15N‐labelled‐leucine from labelled diets. Yolks and post‐ovulatory scales of labelled females were significantly more enriched in 15N than those of unlabelled females in all species, indicating significant assimilation and allocation of income‐derived amino acids to the yolk during vitellogenesis. The lack of among‐species differences suggests that all species allocated income amino acids to vitellogenesis. The results obtained in the present study suggest that proportional utilization of income or capital depends on the frequency and timing of foraging success during reproductive events. Therefore, capital and income breeding may be consequences of both life‐history and environmental constraints on foraging success, rather than strategies of reproductive allocation. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106, 390–404.

Structural and Performance Costs of Reproduction in a Pure Capital Breeder, the Children’s PythonAntaresia childreni

“…Vitellogenic females undergo major physiological changes and mobilize body stores to support the synthesis of vitellogenin and yolk deposition into the growing follicles (Speake et al 2003). Protein breakdown is necessary to provide the essential amino acids required for yolk protein synthesis in the liver (Santos et al 2007;Van Dyke et al 2012). Additionally, vitellogenesis and gravidity impose a significant thermoregulatory shift and a metabolic increase (Lourdais et al 2008).…”

“…Because there was no reproductive end point (e.g., oviposition or hatching) for this group, the final measurements for this group were collected toward the end of oviposition for the two other groups (mean fasting time, d). Fasting du-95.7 ‫ע‬ 0.5 ration in nonreproductive females (group 3) was similar to that in group 1 to quantify the absolute cost of folliculogenesis, which is a primary step of protein allocation into the eggs (Santos et al 2007;Van Dyke et al 2012). Using nonreproducing females rather than true controls (i.e., females that were not allowed to reproduce) potentially confounds results, but we took this approach because all females were of similar body and muscle condition, and randomly allocating females to the three groups would have led to significantly reduced sample sizes for the two reproductive groups (because some females allocated to those groups would have failed to reproduce).…”

“…First, amino acids provide raw materials necessary for subsequent protein synthesis, which is associated with somatic growth and development of the offspring. Considerable amounts of proteins are allocated to the developing embryos via egg yolk (White 1991;Santos et al 2007;Senechal et al 2011;Van Dyke et al 2012) or through postnatal provisioning (e.g., lactation). Also, during prolonged fasting (Lowell et al 1986;Lowell and Goodman 1987;Cherel et al 1992), the conversion of amino acids to glucose via gluconeogenesis is critical.…”

High levels of maternally transferred mercury do not affect reproductive output or embryonic survival of northern watersnakes (Nerodia sipedon)

“…Litter sizes range from 4 to 99 but typically average between 20 and 40 young [16]. Nerodia sipedon are primarily lecithotrophic (embryos nourished by yolk), but there is recent evidence that the placenta present in N. sipedon can transfer nutrients to developing offspring as well as perform respiratory functions [20,21].…”

Female Reproduction inThamnophis scaliger: The Significance of Parturition Timing

“…In species that do not reproduce in sequential years, a female's reproductive output should be mainly a function of her nutritional state acquired over the years prior to reproduction (Gregory, 2006); in contrast, feeding during the calendar year of reproduction affects mostly maternal condition (Gignac and Gregory, 2005). For animals without a placenta, after female ovulation, nutrients acquired from recent food intake theoretically cannot be translated into an increase in offspring size (Ford and Seigel, 2011; see also Van Dyke et al, 2012). Therefore, our results show that feeding during pregnancy only increases postpartum female's body condition.…”