Maternally transferred thyroid hormones and life-history variation in birds.

In vertebrates, thyroid hormones (THs) play an important role in the regulation of growth, development, metabolism, photoperiodic responses and migration. Maternally transferred THs are important for normal early phase embryonic development when embryos are not able to produce endogenous THs. Previous studies have shown that variation in maternal THs within the physiological range can influence offspring phenotype. Given the essential functions of maternal THs in development and metabolism, THs may be a mediator of life-history variation across species. We tested the hypothesis that differences in life histories are associated with differences in maternal TH transfer across species. Using birds as a model, we specifically tested whether maternally transferred yolk THs covary with migratory status, developmental mode and traits related to pace-of-life (e.g. basal metabolic rate, maximum life span). We collected un-incubated eggs (n = 1-21 eggs per species, median = 7) from 34 wild and captive bird species across 17 families and six orders to measure yolk THs [both triiodothyronine (T3) and thyroxine (T4)], compiled life-history trait data from the literature and used Bayesian phylogenetic mixed models to test our hypotheses. Our models indicated that both concentrations and total amounts of the two main forms of THs (T3 and T4) were higher in the eggs of migratory species compared to resident species, and total amounts were higher in the eggs of precocial species, which have longer prenatal developmental periods, than in those of altricial species. However, maternal yolk THs did not show clear associations with pace-of-life-related traits, such as fecundity, basal metabolic rate or maximum life span. We quantified interspecific variation in maternal yolk THs in birds, and our findings suggest higher maternal TH transfer is associated with the precocial mode of development and migratory status. Whether maternal THs represent a part of the mechanism underlying the evolution of precocial development and migration or a consequence of such life histories is currently unclear. We therefore encourage further studies to explore the physiological mechanisms and evolutionary processes underlying these patterns.

Does paternal immunocompetence affect offspring vulnerability to maternal androgens? A study in domestic chickens.

Exposure of yolk androgens can positively stimulate chick growth and competitive ability, but may negatively affect immunity. It has been hypothesized that only chicks from immunologically superior fathers can bear the cost of prenatal exposure to high androgen levels. To test this hypothesis, we paired roosters from two selection lines, one up- and one down-selected for natural antibodies (NAbs), with hens from a control line. We measured yolk testosterone and androstenedione levels, and we injected the treatment group of eggs of each female with testosterone suspended in sesame oil and the control group with sesame oil only. We then measured hatching success and growth, and characterized the humoral and cellular immune responses using three different challenges: a phyto-hemagglutinin, a lipopolysaccharide and a sheep red blood cell challenge. We found that the hatching success, body mass, initial levels of natural antibodies and the chicks' immunological responses to the three different challenges and development were affected neither by paternal immunocompetence nor by treatment. These results do not support the hypothesis that chicks from low-NAb line fathers are more sensitive to testosterone exposure during embryonic development than chicks from high-NAb line fathers.

The relationship between male social status, ejaculate and circulating testosterone concentration and female yolk androgen transfer in red junglefowl (Gallus gallus).

Several studies show that avian females prefer males based on their secondary sexual ornaments and dominance status. We tested in red junglefowl (Gallus gallus) how comb size affected the result of fighting and how the dominance status related to testosterone concentrations in their circulation and ejaculates. We subsequently tested how social status was related to female reproductive investment, including yolk hormone transfer. We found that after a fight 1) winners increased plasma T and decreased ejaculates T whereas losers' T remained unchanged, and 2) plasma T of winners was higher but ejaculates T was lower than those of losers. We argued those are consistent with the different reproductive strategies of dominant and subordinate males. Furthermore, in line with offspring sex-dependent growth patterns females transferred significantly more androstenedione to female than male embryos when mated with winners, while doing the opposite when mated with losers. We concluded therefore that female reproductive investment was affected by both partner quality and embryo sex. The results indicate that male quality influences sex-specific maternal investment, which could be mediated by ejaculate testosterone concentration.

Ejaculate testosterone levels affect maternal investment in red junglefowl (Gallus gallus gallus).

Substantial concentrations of testosterone are not only present in a male's circulation, but also in its ejaculate. Surprisingly, the regulation of ejaculate T and its effects on females and their offspring, potentially a cryptic paternal trait, are not known. We found lower circulating and higher ejaculate T concentrations in subordinate red junglefowl (Gallus gallus gallus) males compared to dominant males, suggestive of an adaptive trade-off in T allocation to circulation and their ejaculate. Subsequently, we artificially inseminated females with either testosterone enriched (TE) or control ejaculates (CE) in a cross-over design. TE females produced heavier eggs than CE females. Offspring growth and tonic immobility were affected in a sex-specific way by TE. TE sons were heavier with shorter TI duration than CE sons, and TE daughters were lighter than CE daughters but daughters did not differ in TI score. However, the chicks competitiveness was not influenced by the TE nor CE. This indicates a previously unknown function of ejaculate testosterone as well as a new form of interaction between a cryptic paternal trait and a maternal effect that may be widespread in the animal kingdom.