The challenge hypothesis: behavioral ecology to neurogenomics

Abstract

Male song sparrows (Melospiza melodia) are territorial year-round. However, neuroendocrine responses to simulated territorial intrusions (STI) differ between breeding (spring) and non-breeding seasons (autumn). In spring, exposure to STI leads to increases in plasma levels of luteinizing hormone and testosterone (consistent with the challenge hypothesis), but not in autumn. This suggests that there are fundamental differences in the mechanisms driving neuroendocrine responses to STI between seasons despite apparently identical behavioral responses. Recent studies have also shown that areas of the telencephalon and diencephalon involved with singing behavior and aggression express the enzymes necessary to synthesize sex steroids de novo from cholesterol. Of these, aromatase (that regulates the conversion of testosterone to estradiol) and 3β-hydroxysteroid dehydrogenase (that regulates the synthesis of biologically active steroids) are regulated seasonally, whereas receptors for sex steroids such as androgen receptor and estrogen receptor alpha and beta are not. Functional analyses indicate specific genes that may be involved in the mechanisms of differential neuroendocrine responses to aggressive interactions in different life-history stages. Microarrays were used to test the hypothesis that gene expression profiles in the hypothalamus after territorial aggression differ between the seasons. Over 150 genes were differentially expressed between spring and autumn in the control birds and 59 genes were significantly affected by STI in autumn, but only 14 genes in spring. Real-time PCR was performed for validation, and it indicated that STI drives differential genomic responses in the hypothalamus in the breeding versus non-breeding seasons. The results suggest major underlying seasonal effects in the hypothalamus that determine the differential response upon social interaction.