Early elevation of testosterone advances migratory preparation in a songbird

Abstract

SUMMARYThe timing of events associated with spring migration can be an important determinant of fitness for migratory birds. The need to prepare and maintain physical condition for migration is one demand that must be met for early arrival on breeding areas, and this demand is compounded by the energetic demands of the physiological transition to breeding. Here, we examined whether migratory birds, specifically males, can adequately meet both of these demands by elevating the sex steroid testosterone early during migratory preparation. To test this, we used a captive experiment in which we photostimulated male dark-eyed juncos (Junco hyemalis) and manipulated circulating testosterone. We predicted males with elevated testosterone would prepare to migrate and breed faster than control males or males where the ability of testosterone to bind with receptors, or be converted to estradiol, was inhibited (testosterone inhibited). We measured migratory preparation using mass, food intake, fat deposits and nocturnal activity (Zugunruhe). To estimate breeding preparation, we measured the diameter of the cloacal protuberance (CP). We found that males in the testosterone treatment group began migratory preparation approximately 10days before controls. There was no difference in the magnitude of peak migratory condition between testosterone-implanted birds and controls. Males implanted with testosterone also reached the onset of breeding preparation faster and had larger peak CP diameter compared with controls. Testosterone-inhibited birds showed no signs of migratory preparation and only a weak increase in CP diameter. These results demonstrate that early elevation of testosterone during migratory preparation could incur benefits for males in terms of the ability to depart earlier from non-breeding areas and arrive in a more advanced breeding condition. This experiment demonstrates that there may be important physiological underpinnings to known winter to breeding season carry-over effects in migratory birds.

Behavioral and physiological traits of migrant and resident White-crowned Sparrows: a common garden approach

“…If one considers onset of migratory restlessness as timing of departure (week 15, Fig. 4A), plasma levels of testosterone and DHT remained unchanged from winter, suggesting that androgens do not regulate the switch from diurnal to nocturnal activity in Z. l. gambelii, as proposed for European starlings (Sturnus vulgaris), dark-eyed juncos and gray catbirds (Dumetella carolinensis) (Owen et al, 2014;Subbaraj and Gwinner, 1985;Tonra et al, 2011). Identifying factors that regulate onset of migratory flight are enigmatic, but the neurosteroid 7α-hydroxypregnenolone may hold promise for its role in the diurnal locomotor activity in Japanese quail (Coturnix japonica) (Tsutsui et al, 2008(Tsutsui et al, , 2012.…”

Increasing photoperiod stimulates the initiation of spring migratory behaviour and physiology in a facultative migrant, the pine siskin

“…Hormone manipulation experiments have provided strong evidence for the role of testosterone in initiating a spring migratory state [7–10], though details about the quantity and timing of androgen secretion necessary to activate migratory physiology and behaviour remain unresolved [61]. In particular, obligate migrants may express a migratory state in spring when circulating levels of androgens are low [62,63], including in species where testosterone has been shown to be important in stimulating migratory physiology and/or behaviour (see control groups in [8,9]). These results suggest that low levels of androgens or a pulse of androgen earlier in the year may be sufficient to initiate spring migratory preparations.…”

Regulatory mechanisms for the development of the migratory phenotype: Roles for photoperiod and the gonad

“…As predicted, this had little effect on either daytime or nighttime activity, which is counter to results others have observed when T is administered along with continuous long photoperiods and suggests that exposure to androgen on short day lengths does not affect migratory restlessness. By contrast, when breeding levels of T are delivered to castrated GWCS, Japanese quail and dark-eyed Juncos under long continuous photoperiods, both reproductive and migratory functions are observed (Tonra et al, 2011;Wada, 1982;Wikelski et al, 1999). This highlights an interaction of photoperiod and androgen but does not elucidate the incremental progression of the spring events.…”

“…Castration completed before but not after the winter solstice prevents the spring day length induced increases in body weight and fat deposition in some (Schwabl and Farner, 1989a;Schwabl et al, 1988;Stetson and Erickson, 1972;Tonra et al, 2011;Weise, 1967) but not all species (Boswell et al, 1993(Boswell et al, , 1995aThapliyal et al, 1983). Whereas these studies document effects of androgens on energy-balancing traits, most of these studies failed to examine the other traits that make up the full migratory sequence.…”

“…In particular, it is important to determine whether, castration delays migratory restlessness or the energetically costly prenuptial molt, an event that precedes migration in the field and may constrain timing of departure in spring (Bauchinger and Biebach, 2006;Pyle, 1997). Finally, most investigations of seasonal traits exposed birds to abrupt changes in day length, a stimulus that differs from the gradual increase in day length that transpires in nature (Lofts and Marshall, 1961;Morton and Mewaldt, 1962;Schwabl and Farner, 1989b;Tonra et al, 2011;Wagner, 1961;Weise, 1967). Abrupt changes in photoperiod might have a telescoping effect on the individual traits leading up to migration, thereby obscuring the actual temporal sequence of endocrine and behavioral events.…”