Variation in maternal effects and embryonic development rates among passerine species

Abstract

Embryonic development rates are reflected by the length of incubation period in birds, and these vary substantially among species within and among geographical regions. The incubation periods are consistently shorter in North America (Arizona study site) than in tropical (Venezuela) and subtropical (Argentina) South America based on the study of 83 passerine species in 17 clades. Parents, mothers in particular, may influence incubation periods and resulting offspring quality through proximate pathways, while variation in maternal strategies among species can result from selection by adult and offspring mortality. Parents of long-lived species, as is common in the tropics and subtropics, may be under selection to minimize costs to themselves during incubation. Indeed, time spent incubating is often lower in the tropical and subtropical species than the related north temperate species, causing cooler average egg temperatures in the southern regions. Decreased egg temperatures result in longer incubation periods and reflect a cost imposed on offspring by parents because energy cost to the embryo and risk of offspring predation are both increased. Mothers may adjust egg size and constituents as a means to partially offset such costs. For example, reduced androgen concentrations in egg yolks may slow development rates, but may enhance offspring quality through physiological trade-offs that may be particularly beneficial in longer-lived species, as in the tropics and subtropics. We provide initial data to show that yolks of tropical birds contain substantially lower concentrations of growth-promoting androgens than north temperate relatives. Thus, maternal (and parental) effects on embryonic development rates may include contrasting and complementary proximate influences on offspring quality and deserve further field study among species.

Hormone-mediated maternal effects in birds:mechanismsmatter but what do we know of them?

“…Yolk androgen and glucocorticoid concentrations respond to artificial selection for behaviour (androgens: Gil & Faure 2007;Groothuis et al submitted;corticosterone: Hayward et al 2005), suggesting the mechanisms of hormone accumulation in the egg as targets for natural selection. Comparative studies show that, among passerine birds, yolk androgen concentrations correlate positively with rate of development (Gorman & Williams (2005); , although in this dataset the correlation was lost after controlling for phylogeny; Schwabl et al (2007); Martin & Schwabl (2008)) and offspring mortality by nest predation (Schwabl et al 2007;Martin & Schwabl 2008) identifying selection pressures. Finally, oestrogens and stress and metabolic hormones are now being studied (oestradiol: Williams et al 2004Williams et al , 2005corticosterone: Hayward & Wingfield 2003;Love et al 2005;Rubolini et al 2005;thyroid hormones: McNabb & Wilson 1997), a timely expansion of a so far myopic focus on the androgen testosterone.…”

“…Consequently, yolk A 4 , T and 5a-DHT can be expected to have different potencies in affecting developmental processes. This is, for example, emphasized by a stronger negative correlation between length of embryo period and yolk 5a-DHT, rather than T concentration among passerine birds (Schwabl et al 2007;Martin & Schwabl 2008). Finally, A 4 may serve as a precursor for T in the embryo, thereby contributing to the pool of the biologically more potent T or 5a-DHT (Groothuis & Schwabl 2002;Schwabl et al 2007) if the conversion enzymes are present in the yolk or embryo.…”

Egg size variation among tropical and temperate songbirds: An embryonic temperature hypothesis

“…Moreover, slower development (i.e., longer embryonic periods) for a constant temperature can allow increased offspring quality and enhanced adult longevity that may be favored in species with slow life history strategies (2,16,26). Indeed, birds show species-specific differences in embryonic periods beyond the variation explained by temperature (16).…”

A trade-off between embryonic development rate and immune function of avian offspring is revealed by considering embryonic temperature

“…Variation in parental incubation behaviour determines temperatures experienced by avian embryos, and experimental swapping of eggs showed that temperature affects length of the embryonic period [9]. Differences in embryonic period owing to such extrinsic effects of temperature do not reflect differences in intrinsic rates of development [10]. Instead, intrinsic rates of embryonic development should be better estimated by deviations from period lengths predicted by embryonic temperature while controlling for any allometric effects of size (figure 1b).…”