Seasonally sympatric but allochronic: differential expression of hypothalamic genes in a songbird during gonadal development

Abstract

Allochrony, the mismatch of reproductive schedules, is one mechanism that can mediate sympatric speciation and diversification. In songbirds, the transition into breeding condition and gonadal growth is regulated by the hypothalamic–pituitary–gonadal (HPG) axis at multiple levels. We investigated whether the difference in reproductive timing between two seasonally sympatric subspecies of dark-eyed juncos ( Junco hyemalis ) was related to gene expression along the HPG axis. During the sympatric pre-breeding stage, we measured hypothalamic and testicular mRNA expression of candidate genes via qPCR in captive male juncos. For hypothalamic mRNA, we found our earlier breeding subspecies had increased expression of gonadotropin-releasing hormone ( GnRH ) and decreased expression of androgen receptor, oestrogen receptor alpha and mineralocorticoid receptor ( MR ). Subspecies did not differ in expression of hypothalamic gonadotropin-inhibitory hormone ( GnIH ) and glucocorticoid receptor ( GR ). While our earlier breeding subspecies had higher mRNA expression of testicular GR , subspecies did not differ in testicular luteinizing hormone receptor, follicle-stimulating hormone receptor or MR mRNA expression levels. Our findings indicate increased GnRH production and decreased hypothalamic sensitivity to sex steroid negative feedback as factors promoting differences in the timing of gonadal recrudescence between recently diverged populations. Differential gene expression along the HPG axis may facilitate species diversification under seasonal sympatry.

Functional Characterization of Three GnRH Isoforms in Small Yellow Croaker Larimichthys polyactis Maintained in Captivity: Special Emphasis on Reproductive Dysfunction

“…However, in three-spined stickleback, a fish expressing two GnRH isoforms, mRNA expression levels of GnRH3 were significantly elevated in spawning fish but downregulated in post-spawning fish [ 36 ], where GnRH3 acts as GnRH1 [ 47 ]. It is believed that reproductive development and gonadal recrudescence are controlled by top-down stimulation of the BPG axis via GnRHs and GtHs with hypothalamic sensitivity to sex steroids providing negative feedback, respectively [ 48 ]. It has also been demonstrated that the capacity of high-affinity GnRH binding sites (presumably representing receptors) might be higher in the breeding season fish than that in the post-breeding season fish [ 49 ].…”

Migratory strategy explains differences in timing of female reproductive development in seasonally sympatric songbirds

“…Migrant and resident male juncos also differ in reproductive timing in common‐garden conditions (Fudickar et al, ). At the end of March, migrant males have significantly smaller testes and lower levels of testosterone than residents, but do not differ in mRNA transcript abundance of reproductive hormone receptors in the testis (Bauer et al, ).…”

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Comparative proteomics reveals molecular correlates of population-level variation in reproductive timing in a North American songbird

“…Prior research on this system using transcriptomics and quantification of specific target genes has shown variation in gene expression in tissues related to the phase lag in the timing of reproduction in migrants as compared to residents, including muscle, blood, and brain (Fudickar et al, 2016a;Bauer et al, 2018;Singh et al, under preparation). But to our knowledge, prior research has not quantified neuroendocrine proteins as a functional correlate for reproductive timing and migratory preparedness.…”