Jodie M. Jawor

MELANIN ORNAMENTS, HONESTY, AND SEXUAL SELECTION

MANY STUDIES OF sexual selection have focused on the role of ornaments in mate choice (see Andersson 1994, Espmark et al. 2000). Birds have been a favorite taxon for those studies because of the prevalence of conspicuous ornaments, including brightly colored feathers, skin, and bills, and dramatically elongated feathers or feathers of elaborate structure. The colors of avian ornaments are the result of carotenoids, melanins, tissue structure, or some combination thereof. Carotenoid ornaments (e.g. bright reds, oranges, and yellows) have generated much interest. Those pigments can not be synthesized de novo by animals, but rather must be included in the diet (Brush 1990). That allows for the possibility that they are limited in nature or diffi cult to obtain (Hill 1994, 1996; Hudon 1994; Linville and Breitwisch 1997). Additionally, carotenoids have been implicated in a variety of critical physiological functions in animals. That recognition has stimulated much recent research on mate choice of carotenoid advertisement and the indicator value of carotenoid ornaments for several important aspects of individual condition. Avian melanin ornaments have also received considerable research attention. In contrast to studies of carotenoid ornaments, however, the primary focus of studies of melanin ornaments has been on the advertisement of melanin “badges” in intrasexual competition. Thus, the associations among expressions of melanin ornaments, mate choice, and individual condition have not been made to the same degree as for carotenoids. There are several possible reasons for that. First, melanins not only color ornaments but are also the basis of most inconspicuous appearances (i.e. camoufl age), in contrast to the highly conspicuous carotenoids. Second, melanins are synthesized by animals and thus do not need to be included in the diet. Finally, it is perhaps incorrectly assumed that melanin ornaments are typically black or blackish-brown and thus show both less variation within species and less diversity across species than do carotenoid ornaments. Here, we review a variety of aspects of the biology of avian melanin ornaments. We demonstrate that the color diversity of melanin ornaments is quite broad, including red (e.g. Red Junglefowl and Barn Swallow [Hirundo rustica]), orange (e.g. Red Junglefowl), yellow (e.g. Western Tanager [Piranga ludoviciana]), and green (e.g. Mallard), in addition to black and brown. Color differences in all melanin ornaments are, in part, a function of the ratio of the two types of melanins contained, and we outline the intriguingly different metabolic pathways to the formation of the two different categories of melanins. There are likely to be both signifi cant physiological benefi ts and costs to melanin production, and those may well differ for the two types of melanins. Finally, we Department of Biology, University of Dayton, Dayton, Ohio 45469-2320, USA JODIE M. JAWOR1 AND RANDALL BREITWISCH MELANIN ORNAMENTS, HONESTY, AND SEXUAL SELECTION The Auk 120(2):249–265, 2003

Natural Variation in a Testosterone‐Mediated Trade‐Off between Mating Effort and Parental Effort

Male birds frequently face a trade‐off between acquiring mates and caring for offspring. Hormone manipulation studies indicate that testosterone often mediates this trade‐off, increasing mating effort while decreasing parental effort. Little is known, however, about individual covariation between testosterone and relevant behavior on which selection might act. Using wild, male dark‐eyed juncos (Junco hyemalis), we measured individual variation in testosterone levels before and after standardized injections of gonadotropin‐releasing hormone (GnRH). The GnRH challenges have been shown to produce short‐term testosterone increases that are similar to those produced naturally in response to social stimuli, repeatable in magnitude, and greater in males with more attractive ornaments. We correlated these testosterone increases with behavioral measures of mating and parental effort (aggressive response to a simulated territorial intrusion and nestling feeding, respectively). Males that showed higher postchallenge testosterone displayed more territorial behavior, and males that produced higher testosterone increases above initial levels displayed reduced parental behavior. Initial testosterone levels were positively but nonsignificantly correlated with aggression but did not predict parental behavior. These relationships suggest that natural variation in testosterone, specifically the production of short‐term increases, may underlie individual variation in the mating effort/parental effort trade‐off. We discuss the implications of these results for the evolution of hormonally mediated trade‐offs.

Natural Selection on Testosterone Production in a Wild Songbird Population

Because of their role in mediating life‐history trade‐offs, hormones are expected to be strongly associated with components of fitness; however, few studies have examined how natural selection acts on hormonal variation in the wild. In a songbird, the dark‐eyed junco (Junco hyemalis), field experiments have shown that exogenous testosterone alters individuals’ resolution of the survival‐reproduction trade‐off, enhancing reproduction at the expense of survival. Here we used standardized injections of gonadotropin‐releasing hormone (GnRH) to assay variation in the testosterone production of males. Using measurements of annual survival and reproduction, we found evidence of strong natural selection acting on GnRH‐induced increases in testosterone. Opposite to what would be predicted from the survival‐reproduction trade‐off, patterns of selection via survival and reproduction were remarkably similar. Males with GnRH‐induced testosterone production levels that were slightly above the population mean were more likely to survive and also produced more offspring, leading to strong stabilizing selection. Partitioning reproduction into separate components revealed positive directional selection via within‐pair siring success and stabilizing selection via extrapair mating success. Our data represent the most complete demonstration of natural selection on hormones via multiple fitness components, and they complement previous experiments to illuminate testosterone’s role in the evolution of life‐history trade‐offs.

Hormones and honest signals: males with larger ornaments elevate testosterone more when challenged.

When male investment in mating varies with quality, reliable sexual signals may evolve. In many songbirds, testosterone mediates mating investment, suggesting that signals should be linked to testosterone production. However, because testosterone may change rapidly during behaviour such as territorial aggression and courtship, efforts to establish such a relationship have proved challenging. In a population of dark‐eyed juncos, we measured individual variation in the production of short‐term testosterone increases by injecting gonadotropin‐releasing hormone (GnRH). We found a positive correlation between the magnitude of these increases and the size of a plumage ornament (‘tail white’) previously shown to be important for female choice and male–male competition. We then measured naturally elevated testosterone levels produced during male–male competition and found that they covaried with those induced by GnRH. We suggest that the association between tail white and testosterone increases may allow conspecifics to assess potential mates and competitors reliably using tail white.

Females competing to reproduce: Dominance matters but testosterone may not

The associations among aggression, testosterone (T), and reproductive success have been well studied, particularly in male birds. In many species, males challenged with simulated or real territorial intrusions increase T and levels of aggression, outcomes linked to higher dominance status and greater reproductive success. For females, the patterns are less clear. Females behave aggressively towards one another, and in some species, females respond to a social challenge with increases in T, but in other species they do not. Prior work on female dark-eyed juncos (Junco hyemalis) had shown that experimental elevation of T increases social status and intrasexual aggression. Here, we conducted two experiments designed to answer three questions: Are endogenous concentrations of T associated with dominance status in captive female juncos? Does dominance status influence readiness to breed in female juncos? And do captive females increase T in response to a challenge? In the first experiment, we introduced two females to a breeding aviary, allowed them to form a dominance relationship and then introduced a male. We found that dominant females were more likely to breed than subordinates, but that dominance status was not predicted by circulating T. In the second experiment, we allowed a resident male and female to establish ownership of a breeding aviary (territory) then introduced a second, intruder female. We found that resident females were aggressive towards and dominant over intruders, but T did not increase during aggressive interactions. We suggest that during the breeding season, intrasexual aggression between females may influence reproductive success, but not be dependent upon fluctuations in T. Selection may have favored independence of aggression from T because high concentrations of T could interfere with normal ovulation or produce detrimental maternal effects.

Natural variation in circulating testosterone does not predict nestling provisioning rates in the northern cardinal, Cardinalis cardinalis

Behavioural transitions between territoriality and parental care are necessary for many seasonally breeding vertebrates. Among birds, such transitions can be mediated by the steroid hormone testosterone (T), resulting in a T-mediated behavioural trade-off. This theory is supported by many implantation studies with birds demonstrating that the administration of exogenous T during parental phases can negatively affect offspring care. However, little is known about relationships between naturally circulating levels of T and parental behaviour in wild bird populations. We examined covariation in circulating levels of T (before and after injection of gonadotropin-releasing hormone (GnRH)) and nestling provisioning rates in male and female northern cardinals, Cardinalis cardinalis, a highly aggressive, biparental resident songbird. Results indicate that both sexes had detectable levels of initial T when providing parental care, but only males produced significantly higher elevations of T following GnRH injections. Furthermore, T levels (both initial and following GnRH injections) and nestling provisioning rates did not covary for either sex, and these measures were not correlated between members of breeding pairs. When results of this study are considered with prior work indicating that elevations in T might not be necessary to support male or female aggression in this species, it appears that relationships between circulating T and reproductive behaviour could be more complex for the cardinal than for many others birds similarly examined. Such findings warrant additional examination of interrelationships between T, aggression and other forms of parental care to assess whether this species engages in T-mediated behavioural trade-offs. Possible alternative mechanisms influencing behaviour in the cardinal and future directions for research are discussed.

TESTOSTERONE IN NORTHERN CARDINALS (CARDINALIS CARDINALIS): POSSIBLE INFLUENCE OF PROLONGED TERRITORIAL BEHAVIOR

Abstract Two attributes of many temperate passerine species are short-term territoriality and strongly fluctuating annual testosterone (T) profiles. Circulating T of temperate passerines can vary from undetectable levels in the nonbreeding season to higher, but fluctuating, levels during the breeding season. Males of many temperate species respond to territorial instability during the breeding season with transitory increases in T. In females, the hormonal response to aggression is more complex. Most temperate-zone passerine species that have been studied exhibit territoriality for less than three months. Here, I describe the year-round T profile of male and female Northern Cardinals (Cardinalis cardinalis), a temperate-zone species with prolonged territorial behavior (7+ months). Circulating levels of T in female Northern Cardinals is relatively stable. Males show variation in T levels over the year and they may respond to territorial intrusions with increases in T. Of particular interest are the relatively high levels of T observed in female Northern Cardinals throughout the year, and measurable amounts of T in both sexes in the winter. Testosterona en Cardinalis cardinalis: Posible Influencia del Comportamiento Territorial Prolongado

Testosterone Elevation and Response to Gonadotropin-Releasing Hormone Challenge by Male Northern Cardinals (Cardinalis cardinalis) Following Aggressive Behavior

There is much discrepancy about the relationship between testosterone (T) and male aggressive behavior. For example, in birds, males of many species significantly elevate T levels during inter-male conflict. However, this is not universal, and in species where males typically do not elevate T during aggressive interactions, concentrations of the hormone are often assumed to be circulating at maximum levels. We examined if male northern cardinals (Cardinalis cardinalis) significantly elevated T during simulated territorial intrusions (STIs). We also examined if individuals had the capacity to further elevate T levels in response to gonadotropin-releasing hormone (GnRH) injections immediately after an aggressive encounter. Our results indicate that male cardinals do not significantly elevate T levels in response to STIs, but have the physiological capacity to significantly elevate T in response to GnRH injections following aggressive interactions. This implies that T levels of individuals captured during STIs were not at maximum concentrations. However, additional findings in this study also suggest the possibility that prolonged social instability could elicit significant elevations in T in males of this species, warranting further investigation.

Non-breeding gonadal testosterone production of male and female Northern Cardinals (Cardinalis cardinalis) following GnRH challenge

Yearly, testosterone (T) levels fluctuate as many vertebrates cycle through reproductive and non-reproductive periods. Among many temperate birds, it is well established that levels of T peak as gonads recrudesce for breeding and then fall as gonads regress prior to the non-breeding season. While the tissues producing breeding season T are well studied, the tissues responsible for non-breeding T have received less investigative attention. We examined the ability of male and female Northern Cardinals (Cardinalis cardinalis) to elevate gonadal T following standardized injections of gonadotropin-releasing hormone (GnRH) across three non-breeding seasons. Males and females were capable of significantly elevating gonadal T production following GnRH injections during periods of reproductive quiescence. The magnitude of T elevation varied across the non-breeding season, but not between sexes. To our knowledge, this is the first report of a significant increase in gonadal T production following GnRH injections administered in the non-breeding season.

Seasonal and sex-related variation in song control nuclei in a species with near-monomorphic song, the northern cardinal.

Studies concerning the song control system (SCS) in songbirds generally focus on males due to their prodigious song production. Both seasonal and age related differences have been found in the size of male SCS regions. Among those studies that have addressed females some level of sexual size dimorphism has been found, with females generally having smaller SCS area than males. Among those species where female song has been studied, typically females either sing much less than males, or they duet with their mates, but in general do not produce independent song. Here we present information on seasonal and sex differences in SCS in the northern cardinal (Cardinalis cardinalis) a species where both sexes sing, females sing independent of their mates, and song is produced by males over a prolonged period of time (7-8 months). We collected brains from free-living adult cardinals, both in the late non-breeding season and during the early breeding season, and measured three song control nuclei; HVC, Area X and RA. There were sex differences in all three areas assessed at the two time points considered. Additionally, there was a seasonal difference in both sexes for all areas assessed. In both time points male SCS nuclei were 1.5-2.0 times larger than female SCS nuclei. These data show that even in those species with independent female song there may still exist sex differences in the SCS nuclei. Similarity in song between the sexes could be related to differences in hormone receptors or hormone levels in the brain, while the small-observed changes in SCS area in males may allow for early breeding season song production and song production outside of the breeding season.