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First evidence for eccentric prealternate molt in the indigo bunting: Possible implications for adaptive molt strategies

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Figure 1.
... Considering that prealternate molts may serve as an adaptation associated with the rigors of migratory behaviors (Howell 2010, Pyle and Kayhart 2010, Wolfe and Pyle 2011, Simpson et al. 2015, Terrill et al. 2020, it is not surprising they appear rare among sedentary Neotropical species. Where prealternate molts do occur among forestdwelling and resident Neotropical landbirds, they appear most common in tanagers (Thraupidae), and to date have been documented in Cyanerpes, Thraupis, Habia, Hemithraupis, Volatinia, Sporophila, Oryzoborus, and Lanio (Dickey and van Rossem 1938, Ryder and Wolfe 2009, Johnson and Wolfe 2017 genera. ...
... obs., Johnson and Wolfe 2017;Myiarchus in Tyrannidae, Pyle 1997, Guallar et al. 2009). Many species in these genera frequent canopies, forest edges, and open grasslands and may sustain a disproportionate amount of feather damage from the sun (Terrill et al. 2020), which is conceptually similar to the hypothetical framework used to explain inserted molts in Nearctic-Neotropic migrants (Pyle 1998, Pyle and Kayhart 2010, Wolfe and Pyle 2011. ...
... However, outside these forests, some African and Australian birds such as widowbirds (Euplectes spp.) and fairywrens (Malurus spp.) are renowned for prealternate molts resulting in dramatic changes in seasonal dichromatism (Mulder andMagrath 1994, Craig 2017). Widowbirds and fairywrens both occur in high ultraviolet environments, which may have led to the evolution of an inserted molt to replace worn plumage, providing an evolutionary opportunity for repurposing by sexual selection--similar to warblers (Parulidae; Kayhart 2010, Wolfe andPyle 2011). In the Neotropics, seedeaters (Sporophila) occur in brushy and sunny environments and often exhibit inserted prealternate molts like those found in widowbirds (although not as extensive) and fairywrens. ...
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The slow-paced life history of many Neotropical birds (e.g., high survival and low fecundity) is hypothesized to increase lifetime fitness through investments in self-maintenance over reproduction relative to their temperate counterparts. Molt is a key investment in self-maintenance and is readily shaped by environmental conditions. As such, variation in molt strategies may be a key mechanism underlying life-history trade-offs and adaptation to new environments. Here, we review molt strategies from a diversity of lowland Neotropical landbirds and examine how variation in molt strategies, characterized by differences in molt insertions, timing, extent, and duration contribute to life-history variation and adaptation to diverse ecological conditions. In addition to our synthesis, we present a case study to examine the relationship between home range size and duration of the definitive prebasic molt of a well-studied subset of Amazonian landbirds. Our results suggest a connection between prolonged molt duration and larger home range size of small-to-medium-sized Amazonian landbirds. Our aims were to identify key gaps in our knowledge of Neotropical bird molt, to stimulate further comparative studies into the evolution of molt strategies, and to highlight how variation in molt strategies may be a key mechanism underlying life-history variation across latitudes.
... Understanding H-P terminology also relies on the premise that evolution has acted to shape molt strategies, and that "plumages" are simply resultant artifacts of molts (Humphrey and Parkes 1959). Thus, although color patterns of feathers may shape the timings and extents of molts once the molts have evolved, the original evolution of an inserted molt in ancestral taxa was likely to replace worn feathers rather than for reasons related to resultant color patterns or other aspects of plumage (Pyle and Kayhart 2010;Wolfe and Pyle 2011). ...
... Similar metabolic processes also appear to occur during ecdysis and/or molt in fish, reptiles, and mammals (King 1972) as well as during the complete prebasic molt (sensu Pyle 2005) of ducks (e.g., Fox and King 2012), suggesting that the prebasic molt may be part of a restoration process ancestral to most or all vertebrates. Such substantive physiological processes may not occur contemporaneously with partial inserted molts, which may have originally evolved in birds simply to replace worn feathers (Pyle and Kayhart 2010;Wolfe and Pyle 2011). Chu (1940) and Höhn (1949) found different patterns of thyroidal activity responding to the separate body molts in Mallards. ...
Article
Humphrey and Parkes (1959) developed a molt and plumage nomenclature (the “H-P” system) based on the evolution of prebasic molts in birds from ecdysis events in reptiles, followed by later evolution of inserted molts responding to lineage-specific constraints and adaptations in Aves. Pyle (2005) revised H-P molt and plumage terminology of ducks by tracing the evolution of their molts from geese, whereas Hawkins (2011) defended traditional molt and plumage terminologies that defined molts relative to present-day breeding seasonality, ensuing plumage coloration, and other proximal factors. Apart from misinterpreting H-P's evolutionary approach, Hawkins (2011) confused the first-cycle terms of H-P, Howell et al. (2003), and Pyle (2005), and presented no new data or ideas to support traditional molt terminology in ducks. It is unlikely that inserted molts evolved in ancestral taxa based on yet-to-occur adaptations involving plumage color, and it is inconsistent to define homologous molts based on similar ensuing feather coloration while disregarding the substantially different coloration of homologous plumages within many avian lineages. Here the terminology of Pyle (2005) is defended, an alternative interpretation for the initial evolution of two (rather than one) inserted molts in the definitive cycles of female and male ducks is elaborated upon, and the future application of metabolic signatures to trace homologous molts in ducks and other bird lineages is suggested. Prebasic molts in ducks and other birds likely evolved from whole-scale restorative events common to all vertebrates, whereas distinguishable and less-comprehensive endocrinological and metabolic processes may accompany inserted molts.
... Although the study of molt and plumages is relatively advanced in North America (Pyle 1997a(Pyle , 1997b, the timing and extent of molts that occur on nonbreeding grounds of Neotropical migrants are not as well known. Several recent studies of common migratory species have revealed more extensive molt than previously known Kayhart 2010, Wolfe andPyle 2011). In addition, previously unknown molts have been detected and described (Dittmann andCardiff 2009, Sieburth and. ...
... The reason behind this prioritization is obscure, although it may have arisen as a solution to reduce flight losses during remex molt, a strategy that could have been selected to reduce predation risk of inexperienced birds in species that need to replace the feathers forming the wingtip during the post-juvenile molt. This view is further supported by the fact that eccentric phenotypes are extremely infrequent in adults (Wolfe & Pyle 2011). Many eccentric phenotypes are heavier than expected but abridged II phenotypes are systematically heavier. ...
Thesis
Molt is the process of plumage renewal by which birds maintain and adjust its functionality throughout their lifecycle. Multiple elements have been tackled in bird molt research (timing, duration, sequence, intensity, extent, feather growth rate, and plumage quality), but major gaps still exist on molt regulation, and especially on molt evolution. This thesis focuses on one molt element extensively recorded since mid-20th century but seldom studied as an individual trait: the set of feathers replaced after a given molt episode by one individual (here referred to as final molt phenotype). This is surprising because feathers differ in their function (e.g. signaling, thermoregulation, contribution to different flight functions, durability), costs of production, and morphology (e.g. exposure, mass, shape), all of which can be targeted by natural selection. Therefore, the final molt phenotype should be under strong selective pressures, suggesting that its regulation has been shaped during evolution to optimize plumage performance throughout the bird’s lifecycle. This thesis explores the potential of analyzing final molt phenotypes as is (instead of being analyzed partially or indirectly) to uncover underlying mechanisms of molt regulation and to provide insights on the evolution of molt in passerine birds. Following are the main findings presented in this thesis. Final molt phenotypes differed between the post-juvenile and the pre-breeding molts along the passerine phylogeny. A nested organization of final molt phenotypes suggested a rank of feather molt importance as underlying rule of molt. However, deviations from perfect nestedness were largely associated with the pre-breeding molt. Shared ancestry explained a large portion of final molt phenotype variation, likely due to constraints associated to plumage morphology, which is highly conserved in passerines. Phylogenetic analyses confirmed the phylogenetic independence of the pre-breeding molt and the strong phylogenetic signal of the post-juvenile molt. Further, they showed the overlooked relevance of environmental factors on the evolution of passerine molt, although their effect varied among taxonomic groups and molt episodes, thus highlighting the flexibility and adaptiveness of molt. Findings exposed in this thesis confirm the relevance of the final molt phenotype as a promising element to advance in our understanding of bird molt.
... Photograph: Ryan S. Terrill that prealternate molts appear to be more common in long-distance migrants than in nonmigratory species and does not always produce plumage color change (Figure 2). Pyle and Kayhart (2010) and Wolfe (2011) observed that a prealternate molt that produces feathers with the same coloration as prebasic molt is a widespread phenomenon in birds and proposed that prealternate molt may not evolve for breeding plumage necessarily. Instead, they proposed that prealternate molt evolves to replace worn feathers and then can be co-opted by pressures for seasonal dichromatism. ...
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Many species of birds show distinctive seasonal breeding and nonbreeding plumages. A number of hypotheses have been proposed for the evolution of this seasonal dichromatism, specifically related to the idea that birds may experience variable levels of sexual selection relative to natural selection throughout the year. However, these hypotheses have not addressed the selective forces that have shaped molt, the underlying mechanism of plumage change. Here, we examined relationships between life‐history variation, the evolution of a seasonal molt, and seasonal plumage dichromatism in the New World warblers (Aves: Parulidae), a family with a remarkable diversity of plumage, molt, and life‐history strategies. We used phylogenetic comparative methods and path analysis to understand how and why distinctive breeding and nonbreeding plumages evolve in this family. We found that color change alone poorly explains the evolution of patterns of biannual molt evolution in warblers. Instead, molt evolution is better explained by a combination of other life‐history factors, especially migration distance and foraging stratum. We found that the evolution of biannual molt and seasonal dichromatism is decoupled, with a biannual molt appearing earlier on the tree, more dispersed across taxa and body regions, and correlating with separate life‐history factors than seasonal dichromatism. This result helps explain the apparent paradox of birds that molt biannually but show breeding plumages that are identical to the nonbreeding plumage. We find support for a two‐step process for the evolution of distinctive breeding and nonbreeding plumages: That prealternate molt evolves primarily under selection for feather renewal, with seasonal color change sometimes following later. These results reveal how life‐history strategies and a birds' environment act upon multiple and separate feather functions to drive the evolution of feather replacement patterns and bird coloration.
... This score measured all body parts of male Indigo Buntings that can potentially exhibit blue plumage colouration including the crown, nape, breast, flanks, belly, back, rump, wing coverts, primary feathers, and tail feathers. Though simple, this visual assessment of the percent of body plumage that is blue has been used in previous studies, both for Indigo Buntings in winter plumage (Wolfe and Pyle, 2011), and closely-related Blue Grosbeaks in nuptial plumage (Keyser and Hill, 2000). T.E.W. was present for the capture and assessment of percent blue for all birds in this study. ...
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Nuptial plumage colouration is seemingly favoured by females of avian species with regards to sexual selection. This particular secondary sexual characteristic has been previously shown to be a condition-dependent signal of individual quality among passerines with pigment-based colouration (i.e. yellows and reds). In contrast, relationships between structural plumage colouration (i.e. blues) and aspects of both physical quality and physiological function have been understudied. Using free-living Indigo Buntings (Passerina cyanea) as a study species, we compared the percentage of blue feather coverage to body condition, innate immune responses, antioxidant capacity, stress physiology, reproductive physiology, and parasitism. We found the overall percentage of blue feathers on individual birds to be positively correlated with testosterone levels and body condition, while negatively correlated with heterophil to lymphocyte ratio. Birds with more blue coverage were also less likely to harbour blood parasites. Our results indicate male Indigo Buntings with greater moult investment have better overall body condition, lower stress, increased testosterone levels, and decreased parasitic susceptibility.
... For example, there appear to be correlations between migratory behavior and the presence and extent of inserted molts. These extra molts may have arisen to mitigate structural damage associated with a migratory lifestyle and subsequently commandeered to reflect honest signals associated with winter-ground quality through changes in plumage coloration (Svensson and Hedenström 1999, Pyle and Kayhart 2010, Wolfe and Pyle 2011. Like other physiological processes and behaviors, molts have presumably resulted from an evolutionary history in which simple adaptations preceded increasingly complex ones. ...
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Howell et al. (2003) published an innovative augmentation to terminology proposed by Humphrey and Parkes (1959) that classified bird molt on the basis of perceived evolutionary relationships. Despite apparent universal applicability, Howell et al.'s (2003) proposed terminological changes were met with criticism that cited a failure to verify the evolutionary relationships of molt and an inability to recognize homologous molts even within closely related taxa. Eleven years after Howell et al. (2003), we revisit arguments against a terminological system of molt based on evolutionary relationships, suggest an analytical framework to satisfactorily respond to critics, clarify terminology, and consider how to study molt variation within an evolutionary framework.
Article
Two broad nomenclatures have emerged to describe moult strategies in birds, the ‘life‐cycle' system which describes moults relative to present‐day breeding and other life‐history events, and the Humphrey–Parkes (H–P) system which reflects the evolution of moults along ancestral lineages. Using either system, challenges have arisen defining strategies in migratory species with more than one moult per year. When all or part of two moults occur in non‐breeding areas, extra moults may fail to be recognized or they may have been discriminated temporally, whether feathers are replaced in fall, winter or spring. But in some cases feather replacement can span the non‐breeding period, and this has resulted in an inability to identify inserted moults and to compare moult strategies between species. Furthermore, recent analyses on factors influencing the extent of the postjuvenile or preformative moults have either confined this moult to the summer grounds or presumed that it can be suspended and resumed on winter grounds, which has lead to quite divergent results and interpretations. Evolutionarily, the timing, extent and location of moults show phenotypic lability whereas the sequence in which feathers are replaced is comparatively conserved. As, such, I propose defining moults on the basis of feather‐replacement sequences as opposed to timing or location of replacement, including strategies in which discrete moults can be suspended for migration and overlap temporally. I provide examples illustrating the functionality of a sequence‐based definition in three migratory North American passerines that can undergo feather replacement twice in non breeding areas, and I demonstrate how this system can effectively apply to moults in many other passerine and non‐passerine species. I recommend that authors studying the evolutionary drivers of moult strategies in migratory birds adopt a sequence‐based approach and to carefully consider replacement strategies both prior to and following autumn migration.
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We document replacement of primaries during the prealternate molt in two and possibly three species of North American gulls of the genus Larus, including the first report of such replacement in an adult Yellow-footed Gull (L. livens), the first report in the Lesser Black-backed Gull (L. fuscus) in the Americas, and possibly the first report for the American Herring Gull (L. argentatus smithsonianus). The incidence and extent of replacement of primaries is greater during the second prealternate than during subsequent prealternate molts, which is likely related to second-cycle molts in Larus being earlier than the subsequent molts. The second prealternate molt of the Lesser Black-backed Gull includes up to all flight feathers (but not all wing coverts). The sequence of replacement of primaries during the prealternate molt matches that of the prebasic molt, starting at the innermost primary and proceeding distally; however, the sequence of replacement of secondaries can differ from that during the prebasic molt, perhaps because of a difference in the underlying mechanisms controlling these molts. Prealternate molt of inner primaries can begin before prebasic molt of outer primaries is completed, a pattern resembling Staffelmauser, but all evidence suggests that the ensuing prebasic molt of the primaries begins at pi, as in terns, rather than at the point where the inner molt wave is suspended, as during Staffelmauser in other large volant birds. We propose that the occurrence and extent of prealternate molt of the remiges in Larus is correlated with the latitude at which an individual winters and/or the timing of the prebasic molt the year before, as much as or more so than with phylogeny. The possible replacement of primaries during the second prealternate molt in North American but not European subspecies of the Herring Gull could relate to some individuals of the American subspecies wintering farther south.
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