Life-history Traits: Delayed Plumage Maturation and Sexual Selection
Two of the most conspicuous life history traits of American Redstarts are:
(1) delayed plumage maturation, in which yearling males look like females (see Appearance) despite their being sexually mature and capable of reproducing successfully; and
(2) strong sexual dimorphism, including both slightly larger bodied males compared to females (Table 1 ; Marra 2000) and dichromatism (i.e., brightly colored, ornamented males compared to more drab females). Larger bodied males compared to females is generally attributed to sexual selection (male-male competition for reproductive opportunities, thus while breeding), but competition for winter territories in redstarts, including competition among females, suggest that the cause of sexual size dimorphism may be more complex in this species, certainly not well understood at present (Webster and Marra 2005).
Delayed maturation extends to song behavior in yearling compared to older males, involving multiple song signals, i.e., both the repeat- and serial-song modes (see Sounds and Vocal Behavior: Vocal Array; Lemon et al. 1994, Germain et al. 2012). Germain et al. 2012 focused for the first time on possible age differences in repeat song mode, in relation to age-related plumage variation. They found statistically different tendencies in repeat song characteristics between yearling and older males. However, within both these age classes the adult-like plumage traits were not correlated with adult-like song traits, suggesting the absence of a single mechanism controlling maturation of both visual and vocal signals. Song behavior is partly learned (see Sounds and Vocal Behavior: Vocalizations) unlike plumage, perhaps explaining the independence of development in these different traits.
Delayed plumage maturation has been studied more extensively than song maturation in American Redstarts, and four hypotheses are proposed to explain the former, including:
(1) mimicry of females to allow tolerance of yearling males within the territories of older males (Rohwer et al. 1980),
(2) cryptic plumage as an antipredator defense (Procter-Gray and Holmes 1981),
All four hypotheses, although not mutually exclusive, find some support in redstarts, or at least remain plausible, but few studies have tested or compared these alternatives critically.
Experimental plucking of selected feathers during the overwintering period indicates that both older and first-winter males regrow feathers with lower red chroma, i.e., less saturation of red coloration consistent with hypothesis (3) of a constraint, possibly related to shortage of dietary sources of carotenoid (including red) pigments (Tonra et al. 2014). Plumage ornamentation terminology, used in this paragraph and below, is based on reflectance spectrometry (e.g., Marini et al. 2015): brightness is reflectance from a feather patch measured across the visible spectrum, 300–700 nm wavelengths; chroma is spectral purity, and red chroma (in redstarts, for example) is purity in the red region, specifically the ratio of reflectance from 605–700 nm divided by that from 300–700 nm; and hue is the color as it appears as determined by the dominant color reflected (e.g., red hue).
The idea of reproductive restraint (hypothesis 4) is supported in redstarts by demographic comparisons (see Demography and Populations: Measures of Breeding Activity): For instance, yearlings, compared with older males, experience on average poorer mating success, smaller clutch size, fewer opportunities for polygynous or extra-pair copulations, fewer opportunities to renest within a season (due to later arrival to breed), reduced fledging success, and reduced assurance of paternity (Ficken and Ficken 1967, Morris and Lemon 1988b, Lemon et al. 1992, Secunda and Sherry 1991, Omland and Sherry 1995, Lozano et al. 1996, S. Perreault, R. E. Lemon, and U. Kuhnlein, unpublished data, TWS). Thus, the ecological factors predisposing redstarts to the evolution of delayed plumage maturation are not well understood, although competition by males for limited mates is probably important (Ficken and Ficken 1967), and yearling males in particular frequently fail to obtain a mate (see Demography and Populations: Annual and Lifetime Reproductive Success). Such competition for limited mates is exacerbated, if not caused, by some combination of facultative polygyny, particularly by older males (Secunda and Sherry 1991, Omland and Sherry 1995, Reudink et al. 2009a), mortality of females associated with the nest site (see Behavior: Predation), and social dominance of males over females on winter territories (Marra et al. 1993), in that this winter competition constrains females to settle in relatively poor-survival winter habitats (Sherry and Holmes 1996a, Marra and Holmes 2001).
The strong sexual dimorphism observed in American Redstarts is indicative of sexual selection. Sexual selection can arise from competition for limited mates and from opportunities to acquire additional partners (polygyny) and extra-pair matings, both of which occur in redstarts as described above. It can also arise from competition for territories in winter. Accordingly, a variety of studies involving redstarts have examined mating and reproductive success in relation to individual variation in traits including plumage, song, and parental care. In yearling males, the extent of black plumage on the head and breast increases with age (see Appearance: Definitive Basic Alternate Plumage). However, controlling for age, first-winter males with more black plumage in the breast area (i.e., look more like older males), tend to hold higher quality winter territories and correspondingly arrive earlier on the breeding grounds, both characteristics that are associated with higher annual survival and higher reproductive success in older males (Germain et al. 2010a, Germain et al. 2010b). One possible explanation for these correlations in yearling males is that ability to fight and defend high quality winter territories causes greater loss of head and breast feathers needing facultative replacement (Germain et al. 2010a). In addition to looking more like adult males, sounding more like them in terms of repeat song mode signaling also appears to confer reproductive advantages at least in adult males, namely likelihood of pairing, earlier nesting, and more young fledged (Germain et al. 2012).
According to sexual selection theory, individuals should gain reproductive advantage from stronger expressions of their ornamental traits, especially in the more ornamented sex. Moreover, yellow, orange, and reddish (structural, carotenoid pigment-based) plumage ornamentation is costly, obtainable only dietarily and unable to be manufactured biochemically in birds (e.g., Marini et al. 2015), which should thus provide an honest signal of fitness. Such ornamentation has been linked in a variety of birds to feeding ability, nutrition, and/or immune system condition. American Redstarts display orange or yellow carotenoid pigments, depending on sex or age (see Appearance) in terms of size or brightness of plumage patches in the flanks, wings, and tail; and a number of studies have correlated this color variation with a variety of behaviors and measures of fitness (reviewed by Marini et al. 2015, and see below).Germain et al. 2010b found that brightness of the flank feathers in redstarts is associated with greater parental care (number of feeding visits to the nest) by males, and nests with more male visits also tend to have more female visits, allowing for the possibility of better fed chicks in such nests (not measured directly). In the same study, females fed less at nests the brighter their mate’s orange tail feathers. Kappes et al. 2009 found that the brightness of orange flank feathers is correlated with pairing success, but none of their carotenoid pigment measures anywhere on the body was correlated with number of offspring sired (based on microsatellite DNA methods), either within the pair bond or with extra-pair matings; and males with more saturated orange flanks (chroma) tended to fledge fewer offspring. Males with brighter flanks fed their nestlings less frequently than duller colored males (Kappes et al. 2009), which is contra to Germain et al. 2010b.
These same orange-red carotenoid pigments (i.e., sexually selected ornamentations) appear to play different signaling roles in American Redstarts, depending on their location on the body and on the ecological context. Specifically, orange flank plumage redness (a function of both red-shifted hue and greater chroma) in older male redstarts is positively correlated with securing and maintaining paternity of offspring at a bird’s own nest (Reudink et al. 2009c), consistent with the Kappes et al. 2009 finding that this trait helps pairing success—all functions associated with intersexual signaling to females. Given this association of paternity and flank redness at a bird’s own nest, achieving extra-pair paternity was negatively associated with flank redness, but positively associated with earlier arrival to the breeding grounds in Spring (see below). In contrast to functions of flank redness, carotenoid feather brightness (red patch) in the tail of older males is correlated positively with polygyny, itself associated with ability to defend multiple breeding territories against other males (Secunda and Sherry 1991) and with the ability to hold preferred winter non-breeding territories (Reudink et al. 2009c, Reudink et al. 2009b)—both of which are associated with intrasexual signaling and male-male competition. Tail feather brightness is associated with winter territory quality, based on a comparison of birds in higher quality (black mangroves) versus lower quality (thorn scrub) habitats in Jamaica (Reudink et al. 2009b; but see Tonra et al. 2014). This finding is reinforced by a stable carbon isotope marker for these two winter habitats that also corresponds with tail feather brightness in a sample of older males captured returning to an Ontario breeding site (Reudink et al. 2009b). The inference from these studies is that the brightness of the red patch in the tail feathers is an important signal of dominance in territorial contests for the best wintering territories, given both the importance of social dominance to winter territoriality (Marra 2000) and the use of the spread tail in territorial displays (see Behavior: Agonistic Behavior).
Tail feather chroma appears to be constrained geographically. Both yearling and older males whose tail feather (r3) had been plucked in winter regrew it with reduced chroma, suggesting a winter dietary constraint that could carry over into the breeding season for individuals who lose rectrices and thus have to replace them during the winter (Tonra et al. 2014; see below). Consistent with this finding, older male redstart tail chroma was stronger in higher latitude breeders and in some breeding zones more than others, either because of dietary carotenoid availability, or possibly variation in parasite loads; but was not related to body condition measured by tail feather daily growth rate (Norris et al. 2007).
Sexual selection depends on the ability of individuals of one sex (males in most birds) to achieve greater genetic fitness than others, leading to the evolutionary exaggeration of traits important in achieving this fitness. In American Redstarts the high variability in individual reproductive fitness (0–8 genetic offspring produced annually (Reudink et al. 2009a) depends not just on the ability to attract a mate and fledge some young as part of a monogamous pair-bond, but also on offspring reared as a result of extra-pair copulation and polygyny (Reudink et al. 2009a). Research on American Redstarts also provides some of the first evidence in any bird that these components of male competition leading to sexual selection depend not just on circumstances around the time of mating and copulation, as widely thought, but also on those in prior seasons; and this research also establishes links between reproduction and winter territoriality in a migratory species. High quality winter territories boost older males’ reproductive success (first-winter males are not well studied in this context), coupled with these individuals’ ability to depart the winter range and arrive to breed early. Specifically, early departure from high quality territories (Marra et al. 1998, Norris et al. 2004a, Reudink et al. 2009a, Cooper et al. 2015) results in higher overall reproductive success (Norris et al. 2004a), greater chance to achieve polygynous matings and extra-pair offspring, and a reduced chance of losing paternity (Reudink et al. 2009a).
Environmental constraints on plumage ornamentation involved in sexual selection are important to interpreting selection pressures favoring the evolution of such ornaments. For example, female choice of older, more experienced males may depend on how plumage changes with age. Long-term studies in Ontario address color changes in individual redstarts’ tail feather (r3) patch (ornamentation) with age, once individuals have attained definitive plumage (orange-red in males two years and older, yellow in females one year and older (Marini et al. 2015). Males tend to have a more orange-shifted hue in their first year definitive adult plumage, becoming slightly yellower with age. The red chroma is highest for males in their second (rather than first or third) years in definitive red-orange plumage. These changes could arise due to differentially accessible dietarily-derived carotenoid pigments, or to intrinsic physiological condition at the time of carotenoid deposition in the feathers. Females in their first breeding season have greater red chroma and lesser brightness than those in their second breeding season, probably due to the timing and conditions of r3 molt (earlier, starting in the nest) for first-time breeders, but also possibly related to diet and body condition (Marini et al. 2015).
Weather can also impact feather ornamentation at the time of molt (Reudink et al. 2015). For example in both individual males and females (across ages) experiencing relatively rainy and possibly warmer July summers (and cooler August), both brightness decreases and redness (defined by both hue and chroma) increases, all these changes deduced to be due to relatively more abundant insects—possibly herbivorous Lepidoptera larvae—in turn providing more dietary precursors of carotenoid pigments (Reudink et al. 2015). Some evidence from this study suggests females respond less strongly to these weather changes than males, perhaps because the former experience different foraging constraints or conditions during molt. These authors suggest that their weather-related effects on rectrix ornaments raise important questions about environment × gene interactions in signaling functions.
Osmond et al. 2013 looked at female carotenoid (yellowish) ornamentation in redstarts, restricting their study to nesting season in Ontario, and to just the bright (yellow) tail and flank ornamental patterns, and not the wing patches. Older females had brighter yellow tail feathers (but not flank) than yearling females. A model with both flank and tail brightness predicted 41% of the variation in yearling female fledging success, brighter females fledging fewer offspring, contrary to prediction. Pairing date, first egg date, and number of young fledged did not differ between yearling and older female age classes. Females with brighter tails fledged fewer young, but just in yearlings, whereas the number of visits older females made to nests declined with tail brightness. Older males made fewer visits to the nests of brighter colored older female mates, and spent less time at the nests based on females’ color brightness, although this relationship was not quite statistically significant. Females with brighter yellow flanks were more likely to mate with males that also had brighter flanks. These correlations of female carotenoid pigments appear to signal individual age—possibly because of the parental influence via feeding behavior on yearling female rectrices—but the other patterns are age-specific, sometimes in opposite direction to the patterns in males, and generally complex and difficult to explain. The causal links among these various relationships needs further study and experimentation.
Osteology And Musculature
In a study of warbler hindlimbs, American Redstarts had a significantly longer third digit (3 proximal phalanges) than that of the Black-throated Green Warbler (Setophaga virens), the most ecologically similar species studied; interpreted as possible advantage in rapid takeoff to capture evasive insects (Osterhaus 1962). Thigh muscles of the redstart have relatively high cross-sectional area relative to the size of the bird, again consistent with their rapid jumping takeoff from perch to pursue insect prey (Commisso 1986). See also Eaton et al. 1963 and Keast et al. 1995.
Angelier et al. 2015 found that telomere length is positively correlated with bill length (but not tarsus length) in first-winter redstarts, suggesting a developmental relationship between bill length and telomere length, which latter is also related to stress, aging, and risk of mortality (see Demography and Populations: Causes of Mortality: Ecological Conditions in Winter).