Maternally Derived Egg Hormones, Antibodies and Antimicrobial Proteins: Common and Different Pathways of Maternal Effects in Japanese Quail

Abstract

Avian eggs contain a variety of maternally-derived substances that can influence the development and performance of offspring. The levels of these egg compounds vary in relation to environmental and genetic factors, but little is known about whether there are correlative links between maternal substances in the egg underlying common and different pathways of maternal effects. In the present study, we investigated genetically determined variability and mutually adjusted deposition of sex hormones (testosterone-T, androstenedione-A4 and progesterone-P4), antibodies (IgY) and antimicrobial proteins (lysozyme) in eggs of Japanese quail (Coturnix japonica). We used different genetic lines that were independently selected for yolk T concentrations, duration of tonic immobility and social reinstatement behaviour, since both selections for behavioural traits (fearfulness and social motivation, respectively) produced considerable correlative responses in yolk androgen levels. A higher selection potential was found for increased rather than decreased yolk T concentrations, suggesting that there is a physiological minimum in egg T levels. Line differences in yolk IgY concentrations were manifested within each selection experiment, but no consistent inter-line pattern between yolk IgY and T was revealed. On the other hand, a consistent inverse inter-line pattern was recorded between yolk IgY and P4 in both selections for behavioural traits. In addition, selections for contrasting fearfulness and social motivation were associated with changes in albumen lysozyme concentrations and an inverse inter-line pattern between the deposition of yolk IgY and albumen lysozyme was found in lines selected for the level of social motivation. Thus, our results demonstrate genetically-driven changes in deposition of yolk T, P4, antibodies and albumen lysozyme in the egg. This genetic variability can partially explain mutually adjusted maternal deposition of sex hormones and immune-competent molecules but the inconsistent pattern of inter-line differences across all selections indicates that there are other underlying mechanisms, which require further studies.

Heritable variation in maternally derived yolk androgens, thyroid hormones and immune factors

“…Previous results on phenotypic variation are controversial; in the study species, a phenotypic correlation between androgens and immune factors was found at between-but not within-clutch level , see also Gasparini et al, 2007), but multiple other studies find no support for the hypothesis (Groothuis et al, 2006;Hargitai et al, 2009;Ruuskanen et al, 2011). In selection lines for yolk T and behavior (quails, Okuliarova et al, 2014), IgY or lysozyme levels did not respond to selection similarly as T, suggesting no genetic covariation. Thus, a similar (or opposite) response to environmental and social conditions could explain the reported phenotypic correlation between yolk androgens and immune factors also in the study species.…”

“…Yolk IgY concentration showed a tendency for low to moderate heritability but this was not statistically significant. Previous data from poultry and quail suggest a heritable basis for maternal IgY and lysozyme transfer (Grindstaff et al, 2003;Abdel-Moneim and Abdel-Gawad, 2006;Okuliarova et al, 2014). The lack of significant heritability for yolk IgY concentration may be due to lack of power (given the large s.e.s).…”

“…Thus parent-offspring conflict and trade-offs between female survival and embryo survival may exist, and selection may be opposite for mothers and offspring. In poultry, artificial selection experiments on immune factors suggest a genetic basis of IgY and lysozyme transfer (Grindstaff et al, 2003;Abdel-Moneim and Abdel-Gawad, 2006;Okuliarova et al, 2014), but there are no studies on their heritability in non-domestic birds.…”

“…Furthermore, high yolk A4 concentrations and low T concentrations were associated with higher maternal lifetime reproductive success ; suggesting that selection acts oppositely on the correlated traits, which would constrain adaptive allocation. Currently, to our knowledge, data on genetic correlations between egg hormones and immunofactors are lacking (but see Okuliarova et al, 2014) and such analyses for any physiological traits in the wild (birds) are scarce (Charmantier et al, 2014). All in all, to understand the evolution of multiple (correlated) egg components and the traits affected by this maternal investment, it is important to study the heritability of different egg components, and their genetic and phenotypic covariation, within a single species and environment.…”

Genetic Divergence in Domestic Japanese Quail Inferred from Mitochondrial DNA D-Loop and Microsatellite Markers

“…Owing to their high growth and egg-laying rates, Japanese quail have been preferentially bred worldwide, including selective breeding to improve egg and meat production, since the beginning of the 20 th century [1]. As quail farming has increased, studies have examined the genetic diversity of domestic quail populations as well as physiological and genetic factors affecting economic traits, such as growth rate, egg-laying rate, and disease resistance [1–6]. Japanese quail is also used in several biological studies as a laboratory animal because of its useful biological properties, including a short generation interval and small body size [7,8].…”