Annual Life History–Dependent Gene Expression in the Hypothalamus and Liver of a Migratory Songbird

Abstract

Birds seasonally switch from one life history state (LHS) to another to maximize their fitness. Accordingly, they exhibit distinct differences in their physiological and behavioral phenotypes between seasons. Possible molecular mechanisms underlying changes through the seasons have scarcely been examined in migratory birds. The present study measured key genes suggested to be involved in the metabolic regulation of 4 photoperiodically induced seasonal LHSs in a long-distance migratory songbird, the blackheaded bunting (Emberiza melanocephala). Buntings were held under short days (8 h light:16 h darkness, 8L:16D), during which they maintained the winter nonmigratory phenotype. Then they were exposed for several weeks to long days (13L:11D). Differences in the activity-rest pattern, body fattening and weight gain, testis size, organ (heart, intestine) weights, and blood glucose and triglyceride levels confirmed that buntings sequentially exhibited spring migration-linked premigratory, migratory, and postmigratory LHSs under long days. The mRNA levels of circadian genes involved in metabolism (Bmal1, Clock, Npas2, Rorα, and Rev-erbα) and of genes that encode for proteins/enzymes involved in the regulation of glucose (Sirt1, FoxO1, Glut1, and Pygl) and lipids (Hmg-CoA; Pparα, Pparγ; Fasn and Acaca) showed LHS-dependent changes in their light-dark expression patterns in the hypothalamus and liver. These initial results on genetic regulation of metabolism in a migratory species extend the idea that the transitions between LHSs in a seasonal species are accomplished by changes at multiple regulatory levels. Thus, these findings promise new insights into the mechanism(s) of adaptation to seasons in higher vertebrates.

Differential gene expression in seasonal sympatry: mechanisms involved in diverging life histories

“…Comparisons of closely related populations of 'seasonally sympatric' migrants and residents can provide a powerful approach to understanding the genetic and physiological bases of traits associated with these stages [3]. Comparative studies have examined expression of candidate genes [4][5][6][7][8][9][10]. However, for complex traits, transcriptomic studies (RNA-seq) have the advantage of capturing a large number of functionally relevant genes that might be missed with a candidate gene approach.…”

Adaptation of oxidative phosphorylation to photoperiod-induced seasonal metabolic states in migratory songbirds

“…A similar role for mdh is suggested in the glucose utilization during reversal of an adult heart to the fetal metabolic pattern in a hypertrophied human heart (Razeghi et al, 2001). It may be noted that buntings have an enlarged heart during the premigratory and migratory phenotypes (Trivedi et al, 2014).…”

“…Group 4 birds, on the other hand, exhibited postmigratory and gonadally regressed (refractory) states with no fat and lean body mass, daytime activity and reproductively inactive testes. Further details of the experiment and results on phenotypic measurements (activity, body mass, fat score and testis size) are recently published (Trivedi et al, 2014).…”

“…The portion of each gene of interest (pdc, pdk, cs, odgh, sdhd and mdh) was cloned and sequenced as described in recent publications from our laboratory Majumdar et al, 2014;Trivedi et al, 2014). Briefly, cDNA was prepared from 1 μg DNase (Promega, M610A) treated RNA (extracted by Tri Reagent solution; Promega, AM9738) using a RevertAid First Strand cDNA Synthesis kit (Thermo Scientific, K1622).…”

“…These birds show daily and seasonal transitions in their physiology and behavior with the onset and end of the migratory seasons (Ramenofsky et al, 1999). In particular, they show hyperphagia, fatten and gain weight, and accumulate carbohydrates and lipids as liver glycogen and adipose tissue triglycerides, respectively, in the days prior to migration (Jain and Kumar, 1995;Jenni and Jenni-Eiermann, 1998;Ramenofsky et al, 1999;McWilliams et al, 2004;Weber, 2009;Singh, 2013;Trivedi et al, 2014). These metabolic reserves are catabolized to provide inflight fuels during migration.…”