Seasonal differences in hypothalamic thyroid‐stimulating hormone β, gonadotropin‐releasing hormone‐I and deiodinase expression between migrant and resident subspecies of white‐crowned sparrow (Zonotrichia leucophrys)

Abstract

Across taxa, the seasonal transition between non-breeding and breeding states is controlled by localised thyroid hormone signalling in the deep brain via reciprocal switching of deiodinase enzyme expression from type 3 (DIO3) to type 2 (DIO2). This reciprocal switch is considered to be mediated by increasing thyroid-stimulating hormone β (TSHβ) release from the pars tuberalis, which occurs in response to a change in photoperiod. Although well characterised in a handful of model organisms in controlled laboratory settings, this pathway remains largely unexplored in free-living animals under natural environmental conditions. In this comparative gene expression study, we investigated hypothalamic thyroid hormone signalling in two seasonally breeding subspecies of white-crowned sparrow (Zonotrichia leucophrys), across the entirety of their annual cycles. The migratory Gambel's (Z. l. gambelii) and resident Nuttall's (Z. l. nuttalii) subspecies differ with respect to timing of reproduction, as well as life history stage and migratory strategies. Although DIO3 mRNA expression was elevated and DIO2 mRNA expression was reduced in the wintering period in both subspecies, DIO2 peaked in both subspecies prior to the onset of reproduction.However, there was differential timing between subspecies in peak DIO2 expression. Intriguingly, seasonal modulation of TSHβ mRNA was only observed in migrants, where expression was elevated at the start of breeding, consistent with observations from other highly photoperiodic species. There was no correlation between TSHβ, DIO2 and gonadotropin-releasing hormone-I mRNA or reproductive metrics in residents. Based on these observed differences, we discuss potential implications for our understanding of how changes in medial basal hypothalamic gene expression mediates initiation of seasonal reproduction.

Light receptors in the avian brain and seasonal reproduction

“…Concurrent with the increase in DIO2 expression, there is a decrease in type 3 deiodinase (DIO3) expression. This reciprocal switch in hypothalamic deiodinase expression between long and short photoperiods has been confirmed in a number of seasonal breeders (Borah et al, 2022;Nakao et al, 2008;Pérez et al, 2021;Stevenson & Ball, 2012;Wang et al, 2019;Yasuo et al, 2005). Deiodinase enzymes are key regulators of thyroid hormones with DIO3 acting to inactivate both bioactive triiodothyronine (T3) and thyroxine (T4), while DIO2 serves as an activating enzyme converting T4, abundant in circulation but low bioactivity, into bioactive T3.…”

“…rapid switches from non‐stimulatory to stimulatory photoperiods over a 24‐h period). However, emerging data utilizing natural changes in photoperiod and/or a wider array of focal species is providing powerful contrasting information from real‐life physiological scenarios (Bentley et al, 2013; Pérez et al, 2021; Wang et al, 2019). While, these studies broadly support the general paradigm of photoinduction of seasonal reproduction, particularly the role of deiodinase switching in the MBH, they do call into question that canonical linkage between changes in TSHβ expression and reciprocal changes in deiodinase expression, which merit further study.…”

Gene expression of sex steroid metabolizing enzymes and receptors in the skeletal muscle of migrant and resident subspecies of white-crowned sparrow (Zonotrichia leucophrys)

“…(Weckstein, Zink et al 2001). In addition, hormone profiles appear to have diverged with residents having lower circulating hormones during breeding (Krause, Németh et al 2016, Krause, Németh et al 2021, Perez, Krause et al 2021. We collected pectoralis muscle because it is critical for flight and gastrocnemius muscle which is important for terrestrial locomotion.…”