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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.

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We investigated time course of photoperiodically driven transcriptional responses in physiologically contrasting seasonal life-history states in migratory blackheaded buntings. Birds exhibiting unstimulated winter phenotype (photosensitive state; responsive to photostimulation) under 6-h short days, and regressed summer phenotype (photorefractory state; unresponsiveness to photostimulation) under 16-h long days, were released into an extended light period up to 22 h of the day. Increased tshβ and dio2, and decreased dio3 mRNA levels in hypothalamus, and low prdx4 and high il1β mRNA levels in blood confirmed photoperiodic induction by hour 18 in photosensitive birds. Further, at hours 10, 14, 18 and 22 of light exposure, the comparison of hypothalamus RNA-Seq results revealed transcriptional differences within and between states. Particularly, we found reduced expression at hour 14 of transthyretin and proopiomelanocortin receptor, and increased expression at hour 18 of apolipoprotein A1 and carbon metabolism related genes in the photosensitive state. Similarly, valine, leucine and isoleucine degradation pathway genes and superoxide dismutase 1 were upregulated, and cocaine- and amphetamine-regulated transcript and gastrin-releasing peptide were downregulated in the photosensitive state. These results show life-history-dependent activation of hypothalamic molecular pathways involved in initiation and maintenance of key biological processes as early as on the first long day.

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Twice-a-year, large-scale movement of billions of birds across latitudinal gradients is one of the most fascinating behavioral phenomena seen among animals. These seasonal voyages in autumn southwards and in spring northwards occur within a discrete time window and, as part of an overall annual itinerary, involve close interaction of the endogenous rhythm at several levels with prevailing photoperiod and temperature. The overall success of seasonal migrations thus depends on their close coupling with the other annual sub-cycles, namely those of the breeding, post-breeding recovery, molt and non-migratory periods. There are striking alterations in the daily behavior and physiology with the onset and end of the migratory period, as shown by the phase inversions in behavioral (a diurnal passerine bird becomes nocturnal and flies at night) and neural activities. Interestingly, there are also differences in the behavior, physiology and regulatory strategies between autumn and spring (vernal) migrations. Concurrent molecular changes occur in regulatory (brain) and metabolic (liver, flight muscle) tissues, as shown in the expression of genes particularly associated with 24 h timekeeping, fat accumulation and the overall metabolism. Here, we present insights into the genetic basis of migratory behavior based on studies using both candidate and global gene expression approaches in passerine migrants, with special reference to Palearctic-Indian migratory blackheaded and redheaded buntings.