Ambient temperature affects multiple drivers of physiology and behaviour: adaptation for timely departure of obligate spring migrants

Abstract

We investigated the role of ambient temperature in departure from wintering areas of migratory blackheaded buntings in spring. Birds transferred at 22 and 35 oC temperatures to long days were compared with one another and to controls held on short days for indices of readiness to migrate (Zugunruhe, fattening, weight gain), levels of testosterone, and gonadal recrudescence. Temperature affected the development of migratory behaviour and physiology: buntings under long days at 35oC, compared to those at 22oC, showed altered migratory behaviour (daily activity and Zugunruhe onset), and enhanced muscle growth and plasma testosterone levels; however, no effect on testis growth. Temperature was perceived at both peripheral and central levels, and affected multiple molecular drivers culminating into the migratory phenotype. This was evidenced by post-mortem comparison of the expression of 13 genes with known functions in the skin (temperature-sensitive TRP channels: trpv4 and trpm8), hypothalamus and/ or midbrain (migration-linked genes: th, ddc, adcyap1 and vps13a) and flight muscles (muscle growth associated genes: ar, srd5a3, pvalb, mtor, myod, mstn and hif1a). In photostimulated birds, the expression of trpv4 in skin, of th in hypothalamus and midbrain, and of srd5a3, ar pvalb and mtor genes in flight muscle, in parallel with T levels, was greater at 35oC than the 22oC. These results demonstrate the role of ambient temperature in development of the spring migration phenotype, and suggest that transcriptional responsiveness to temperature is a component of the overall adaptive strategy in latitudinal songbird migrants for timely departure from wintering areas in spring.

Genetic Control of Avian Migration: Insights from Studies in Latitudinal Passerine Migrants

“…The Tshb - Dio2 - Gnrh gene pathway was upregulated at a high temperature (38 °C), while expression of the Trpm8 gene (encoding for transient receptor potential cation) was found to be high at 22 °C, compared to 38 °C (TRPM8 is known to be activated in response to ∼8–25 °C temperature; [ 71 ]). In a similar experiment also on migratory blackheaded buntings, both cutaneous and hypothalamic expressions of the Trpv4 gene which senses warm temperatures (∼27–37 °C) were upregulated at 35 °C ( Figure 2 , [ 67 ]).…”

“…The reduced Th mRNA levels in castrates, compared to intact buntings, further supports this [ 89 ]. Interestingly, the expression of Th is modulated by the light quality and temperature suggesting a functional interaction of the hypothalamic thermosensitive and photoreceptive cells with dopaminergic neurons [ 67 , 90 ]. Photostimulated redheaded buntings showed higher hypothalamic Th mRNA levels when they were exposed to a short light wavelength (460 nm), compared to when they were exposed to a longer light wavelength (620 nm) [ 90 ].…”

“…Photostimulated redheaded buntings showed higher hypothalamic Th mRNA levels when they were exposed to a short light wavelength (460 nm), compared to when they were exposed to a longer light wavelength (620 nm) [ 90 ]. Likewise, the exposure to a stimulatory photoperiod at 35 °C led to an increased Th mRNA expression, compared to levels at 22 °C, in both the midbrain and hypothalamus of migratory blackheaded buntings ( Figure 2 , [ 67 ]).…”

Differential regulatory strategies for spring and autumn migrations in Palearctic-Indian songbird migrants

“…Post vernal equinox period, the overwintering birds begin to prepare for their northward migratory travel in response to increasing spring photoperiods (≥12 h daily light); the converse is true for the post autumn equinox period when birds respond to a decreasing photoperiod despite it being still close to the threshold for photoperiodic induction in spring. The ambient temperature also plays a crucial role in the development of the migration phenotype, as evidenced by transcriptional response to temperature in the development of spring migratory phenotype in captive redheaded buntings ( Sur et al, 2020 ). The decision for migratory departure is, therefore, the outcome of the integration of environmental photoperiod and temperature with the migratory context (to breeding grounds in spring and to wintering areas in autumn) and the physiological state (pre-reproductive state in spring vs. post-reproductive state in autumn).…”

Photoperiod-driven concurrent changes in hypothalamic and brainstem transcription of sleep and immune genes in migratory redheaded bunting

“…The development of vernal migratory phenotype (body fattening, weight gain and nocturnal Zugunruhe) and departure timing can be reproduced under semi-natural photoperiod and ambient temperature in buntings [24]. Similarly, photostimulated vernal migratory and breeding states can be induced in buntings exposed to artificial stimulatory photoperiodic conditions [25–27]. Thus, we induced four different LHS by changing the photoperiodic conditions, and monitored the activity, sleep–wake cycle, general physiology, and measured the mRNA expression of candidate genes involved in sleep homeostasis.…”