American Society of Naturalists

A membership society whose goal is to advance and to diffuse knowledge of organic evolution and other broad biological principles so as to enhance the conceptual unification of the biological sciences.

“Between- and within-individual variation of maternal thyroid hormone deposition in wild great tits (Parus major)”

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Bin-Yan Hsu, Irene Verhagen, Phillip Gienapp, Veerle M. Darras, Marcel E. Visser, and Suvi Ruuskanen (Oct 2019)

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How much flexibility do mothers have to alter the early environment of their offspring?

Eggs of great tit (<i>Parus major</i>). This photo was taken in Ruissalo, Finland, on May 3rd, 2019, by the photographer Pierre-Lou Chapot, <a href="https://www.pierrelouchapot.com/home">www.pierrelouchapot.com/home</a>
Eggs of great tit (Parus major). This photo was taken in Ruissalo, Finland, on May 3rd, 2019, by the photographer Pierre-Lou Chapot, www.pierrelouchapot.com/home

During breeding, some hormones are transferred from mothers to their offspring. These maternal hormones can influence the development, growth, physiology, and also behavior of the offspring. Evolutionary biologists have hypothesized that maternal hormones may be a “tool” for mothers to help their offspring adapt to the future environment after birth. To achieve this task, however, mothers must be able to adjust the amounts of hormone they transfer to their offspring. Can they do that?

In this study, Hsu, Verhagen, Gienapp, Darras, Visser, and Ruuskanen chose the great tits (Parus major), a small passerine bird in Europe, as a model to study the flexibility of maternal hormone transfer. In birds, mothers transfer and store maternal hormones in the egg yolks. The authors analyzed the variation of maternal thyroid hormones in the eggs sampled from a Dutch population during 2013-2016. In all vertebrates, two thyroid hormones – triiodothyronine (T3) and thyroxine (T4) – are considered important to many physiological functions, such as development and metabolism. The analysis suggests that different females transfer different levels of T3 to the egg yolks on average. By contrast, each female bird is capable of adjusting T4 transfer differently for each clutch of eggs, thus potentially influencing the phenotype of the chicks and the degree of competition between the siblings hatching from these eggs. Because a previous study has shown that genetics has a moderate control over maternal T3 but not T4, this study shows that the two forms of maternal thyroid hormones exhibit different patterns of variation and flexibility, which may be linked to their respective functions.


Abstract

Maternal hormones are often considered a mediator of anticipatory maternal effects, namely mothers adjust maternal hormone transfer to prepare the offspring for the anticipated environment. The flexibility for mothers to adjust hormone transfer is therefore a prerequisite for such anticipatory maternal effects. Nevertheless, previous studies have only focused on the average differences of maternal hormone transfer between groups and neglected the substantial individual variation, despite that individual plasticity in maternal hormone transfer is actually the central assumption. In this study, we studied the between- and within-individual variation of maternal thyroid hormones (THs) in egg yolk of wild great tits (Parus major) and estimated the individual plasticity of maternal yolk THs across environmental temperature, clutch initiation dates and egg laying order using linear mixed-effects models. Interestingly, our models provide statistical evidence that the two main THs – the main biologically active hormone T3, and T4, which is mostly considered as a prohormone – exhibited different variation patterns. Yolk T3 showed significant between-individual variation on the average levels, in line with its previously reported moderate heritability. Yolk T4, however, showed significant between-clutch variation in the pattern over the laying sequence, suggesting a great within-individual plasticity. Our findings suggest that the role and function of the hormone within the endocrine axis likely influences its flexibility to respond to environmental change. Whether the flexibility of T4 deposition brings fitness advantage should be examined along with its potential effects on offspring, which remains to be further investigated.