Manipulation of Prenatal Thyroid Hormones Does Not Affect Growth or Physiology in Nestling Pied Flycatchers

Abstract

Hormones transferred from mothers to their offspring are thought to be a tool for mothers to prepare their progeny for expected environmental conditions, thus increasing fitness. Thyroid hormones (THs) are crucial across vertebrates for embryonic and postnatal development and metabolism. Yet yolk THs have mostly been ignored in the context of hormonemediated maternal effects. In addition, the few studies on maternal THs have yielded contrasting results that could be attributed to either species or environmental differences. In this study, we experimentally elevated yolk THs (within the natural range) in a wild population of a migratory passerine, the European pied flycatcher (Ficedula hypoleuca), and assessed the effects on hatching success, nestling survival, growth, and oxidative status (lipid peroxidation, antioxidant enzyme activity, and oxidative balance). We also sought to compare our results with those of a closely related species, the collared flycatcher (Ficedula albicolis), that has strong ecological and life-history similarities with our species. We found no effects of yolk THs on any of the responses measured. We could detect only a weak trend on growth: elevated yolk THs tended to increase growth during the second week after hatching. Our results contradict the findings of previous studies, including those of the collared flycatcher. However, differences in fledging success and nestling growth between both species in the same year suggest a contextdependent influence of the treatment. This study should stimulate more research on maternal effects mediated by THs and their potential context-dependent effects.

Testing for context-dependent effects of prenatal thyroid hormones on offspring survival and physiology: an experimental temperature manipulation

“…2 e,f, Supplementary Tables S6 , S7 ). These results support our previous findings where elevated prenatal THs did not appear to influence postnatal oxidative stress biomarkers in birds 16 , 17 . Yet, effects of prenatal THs on oxidative stress could be tissue-dependent and/or only visible during embryo development, which needs to be further tested.…”

“…2 a, Supplementary Tables S2 , S3 ). Our results therefore suggest that the previously reported discrepancies in the effects of prenatal THs on offspring growth across sister species (collared and pied flycatchers 16 , 17 ), and other altricial birds 18 , 44 are unlikely driven by context-dependent effects of THs related to early postnatal temperature differences. Yet, there are several possible alternative explanations: (1) the study took place in a relatively warm year, with the average temperature during the nestling phase (June-July) being ca.…”

“…We conducted our experiment in a nest-box population of pied flycatchers located in Turku, Finland (60° 25′ N, 22° 10′ E). Egg THs were manipulated in unincubated eggs using injections in the yolk, following the procedure in 17 . The dose was based on the average (± SD) yolk T3 and T4 levels we previously measured from the same population of pied flycatcher eggs (N = 15, T3 = 0.740 ± 0.238 ng/yolk, T4 = 2.307 ± 0.654 ng/yolk).…”

“…Two randomly picked samples per nest were selected due to logistical constraints. Two oxidative stress biomarkers, (1) oxidative damage to lipids (malondialdehyde, MDA, nmol/mg protein, using TBARS assay) and (2) total glutathione (hereafter tGSH; µmol GSH/mg protein), the most abundant endogenous intracellular antioxidant, were measured using established protocols, with all intra-assay CVs < 10%, following 17 . For oxidative stress biomarkers, we excluded the nests whose nestlings were not involved in cross-fostering and the numbers of nestlings analyzed were 179 and 155 at d8 and d13, respectively.…”

“…We previously reported contrasting effects of maternal thyroid hormones (THs: T3 = triiodothyronine, T4 = thyroxine) on offspring phenotype in two closely related species, the collared flycatcher ( Ficedula albicollis ) and pied flycatcher ( F. hypoleuca ) 16 , 17 . THs increased early growth, but decreased growth during the second week post-hatching in collared flycatchers 16 , while they tended to increase growth during the second week post-hatching in pied flycatchers 17 . The underlying mechanisms and the explanations for these contrasting results remain unknown, but one hypothesis could be that the effects of elevated yolk THs would depend on the post-hatching environmental conditions.…”