Zonotrichia Albicollis Research Articles

Stopover refuelling, movement and departure decisions in the white-throated sparrow: The influence of intrinsic and extrinsic factors during spring migration.

Differential migration timing between sex or age classes is an example of how migratory movement strategies can differ among subgroups within a population. However, in songbirds, evidence for intrinsic differences in en route migratory behaviour is often mixed, suggesting that the local environmental context may play a role in accentuating or diminishing patterns. We evaluated how multiple intrinsic and extrinsic variables influenced refuelling rates, local movement behaviour and departure decisions in the white-throated sparrow Zonotrichia albicollis during spring migration. This species exhibits a unique genetically based plumage dimorphism, providing a unique class of individual in which to evaluate patterns and processes of differential migration, in addition to sex, age and migration distance. At a migratory stopover site, plasma metabolite analysis was used to quantify individual variation in stopover refuelling rate. In after second year adults, automated and manual radio telemetry was used to quantify daily activity timing, daily movement distances, stopover duration and departure time. Arrival timing to the stopover site was determined using capture data. Non-breeding and previous breeding/natal latitude were determined using analysis of hydrogen isotopes in claws and feathers. Males arrived at the stopover site 11days on average before females, but no difference in migration timing was observed between plumage morph or age classes. After second year, adults with more southern previous breeding latitudes arrived at stopover earlier, whereas second year birds making their first return migration arrived at stopover in an inverse relationship to non-breeding latitude. Stopover refuelling rate did not differ between ages, sexes or plumage morphs, and daily departure probability of adults was higher under warmer temperatures and favourable tailwinds. White-striped morphs moved greater distances during stopover, initiated daily activity earlier in the morning and departed for migration earlier in the evening than tan-striped morphs. Our results show that while individual phenotype can influence some aspects of local stopover-scale movement behaviour, evidence for differential stopover behaviour was weak. Differential migration timing is unlikely to result from intrinsic differences in en route refuelling rate and departure decisions, especially because the latter is strongly influenced by meteorological conditions.

A supergene-linked estrogen receptor drives alternative phenotypes in a polymorphic songbird

Behavioral evolution relies on genetic changes, yet few behaviors can be traced to specific genetic sequences in vertebrates. Here we provide experimental evidence showing that differentiation of a single gene has contributed to the evolution of divergent behavioral phenotypes in the white-throated sparrow, a common backyard songbird. In this species, a series of chromosomal inversions has formed a supergene that segregates with an aggressive phenotype. The supergene has captured ESR1, the gene that encodes estrogen receptor α (ERα); as a result, this gene is accumulating changes that now distinguish the supergene allele from the standard allele. Our results show that in birds of the more aggressive phenotype, ERα knockdown caused a phenotypic change to that of the less aggressive phenotype. We next showed that in a free-living population, aggression is predicted by allelic imbalance favoring the supergene allele. Finally, we identified cis-regulatory features, both genetic and epigenetic, that explain the allelic imbalance. This work provides a rare illustration of how genotypic divergence has led to behavioral phenotypic divergence in a vertebrate.

Animal Culture: How a New Birdsong Went Viral

A new white-throated sparrow song has overtaken most of Canada in less than 20 years. The explanation for this remarkably fast spread may lie in the southern migratory grounds, where populations from across Canada converge each winter.

High Rates of Exposure to Simulated Winter Storm Cues Negatively Affect White-Throated Sparrow (Zonotrichia albicollis) Energy Reserves

Climate change is causing changes in weather patterns and more frequent extreme weather events. Although birds are often able to cope with and respond to inclement weather with physiological and behavioral responses, as weather events become more severe or frequent the adaptive coping responses of many species may be pushed beyond their limits. We investigated the effects of experimental recurrent inclement winter weather cues on body composition, glucocorticoid hormones, and behavior of white-throated sparrows (Zonotrichia albicollis). We used a hypobaric climatic wind tunnel to simulate storms by transiently decreasing barometric pressure and temperature, and measured behavioral responses, body composition, and baseline corticosterone levels in birds exposed, or not exposed (control), to different frequencies of simulated storms. In study 1, experimental birds were exposed to one storm per week over 9 weeks. In study 2, experimental birds were exposed to two storms per week over 12 weeks. Birds exposed to one simulated storm per week had higher fat and lean masses than control birds, with no differences in the amount of time groups spent feeding. This change in body composition suggests that birds were coping by increasing energy stores. In contrast, birds exposed to two simulated storms per week had lower fat masses compared to control birds, even though they spent more time feeding. Experimental birds in study 2 also had lower baseline corticosterone levels than controls. These changes suggest that the coping response observed in study 1 was overcome in study 2. These findings provide novel experimental evidence that birds detect and respond to changes in temperature and barometric pressure independent of other storm-related cues. One simulated storm per week resulted in potentially adaptive responses of increase mass. However, increasing the frequency of storm exposure to twice per week may exceed a physiological threshold for tolerance to which these songbirds are able to cope. These results also experimentally demonstrate that repeated exposure to inclement weather cues can directly affects birds’ energy reserves, with strong implications for survival as severe weather events continue to become more prevalent.

Continent-wide Shifts in Song Dialects of White-Throated Sparrows

Hypotheses on regional song variation ("dialects") assume that dialects remain stable within regions, are distinct between regions, and persist within populations over extensive periods [1-3]. Theories to explain dialects focus on mechanisms that promote persistence of regional song variants despite gene flow between regions [4-6], such as juveniles settling in non-natal populations retaining only those songs from their repertoires that match neighbors [7, 8]. It would be considered atypical for a novel song variant to invade and replace the established regional variant. Yet some studies have reported song variants shifting rapidly over time within populations [9-11]. White-throated sparrows, Zonotrichia albicolis, for example, traditionally sing a whistled song terminating in a repeated triplet of notes [12], which was the ubiquitous variant in surveys across Canada in the 1960s [13]. However, doublet-ending songs emerged and replaced triplet-ending songs west of the Rocky Mountains sometime between 1960 and 2000 [11] and appeared just east of the Rockies in the 2000s [14]. From recordings collected over two decades across North America, we show that doublet-ending song has now spread at a continental scale. Using geolocator tracking, we confirm that birds from western Canada, where doublet-ending songs originated, overwinter with birds from central Canada, where the song initially spread. This suggests a potential mechanism for spread through song tutoring on wintering grounds. Where the new song variant has spread, it rose from a rare variant to the sole, regional song type, as predicted by the indirect biased transmission hypothesis [10]. VIDEO ABSTRACT.

Behavioural polymorphism in wintering white-throated sparrows, Zonotrichia albicollis

Behavioural polymorphisms associated with morphs with a known genetic basis are interesting to study since they provide a model system to investigate the molecular basis of complex behaviours. White-throated sparrows are one of such rare models, presenting two morphologies and behavioural types, tan and white, caused by a chromosomal rearrangement. The behavioural differences have been mainly studied during reproduction, defining two morph-specific breeding strategies and different levels of aggression between morphs. Outside of the breeding season, the morphological differences are less apparent, morphs are more difficult to distinguish and the behavioural polymorphism is poorly understood. In this study, we caught wild individuals during the winter, determined their morph by genetic analysis, and analysed the differences in behaviour between morphs when encountering a novel object under standardized conditions in captivity. White morphs are more aggressive during reproduction; therefore, we expected them to be less affected by the presence of the novel object than tan morphs; animal personality research shows that more aggressive individuals are less affected by the presence of novel objects (i.e. neophilic). Contrary to our expectations, white morphs were more neophobic than tan morphs, and within morphs, males were more neophobic than females. Furthermore, white morph individuals and males of both morphs suffered greater weight loss during captivity compared to tan morphs and females, respectively, suggesting that the response to captivity-induced stress differs between morphs and between sexes. Finding behavioural differences between morphs not related to reproduction implies a broader impact of the effects of the chromosomal rearrangement on the behavioural polymorphism in this species.

Vasoactive intestinal peptide as a mediator of the effects of a supergene on social behaviour.

Supergenes, or linked groups of alleles that are inherited together, present excellent opportunities to understand gene-behaviour relationships. In white-throated sparrows (Zonotrichia albicollis), a supergene on the second chromosome associates with a more aggressive and less parental phenotype. This supergene includes the gene for vasoactive intestinal peptide (VIP), a neuropeptide known to play a causal role in both aggression and parental behaviour. Here, using a free-living population, we compared the levels of VIP mRNA between birds with and without the supergene. We focused on the anterior hypothalamus and infundibular region, two brain regions containing VIP neurons known to play a causal role in aggression and parental behaviour, respectively. First, we show that the supergene enhances VIP expression in the anterior hypothalamus and that expression positively predicts vocal aggression independently of genotype in both sexes. Next, we show that the supergene reduces VIP expression in the infundibular region, which suggests reduced secretion of prolactin, a pro-parental hormone. Thus, the patterns of VIP expression in these two regions are consistent with the enhanced aggression and reduced parental behaviour of birds with the supergene allele. Our results illustrate mechanisms by which elements of genomic architecture, such as supergenes, can contribute to the evolution of alternative behavioural phenotypes.

Experimental Malaria Infection Affects Songbirds' Nocturnal Migratory Activity.

Migratory animals encounter multiple parasite communities, raising concerns that migration may aid transport of infectious disease. How migration affects disease spread depends fundamentally on how disease affects migration, specifically whether infection alters individuals' migratory physiology and behavior. We inoculated white-throated sparrows (Zonotrichia albicollis) with avian malaria parasites (Plasmodium sp.), monitored parasite loads for 5 wk as the birds reached spring migratory condition, and compared nocturnal migratory restlessness (Zugunruhe), body composition (fat, lean, and whole-body mass), and hematocrit among experimentally infected birds, sham-inoculated birds, and birds that were exposed to parasites but resisted infection. Migratory restlessness increased over time in the study, but the rate of change varied between sham (control) birds, infected birds, and birds that resisted infection. We were unable to detect any effects of malaria exposure on body condition. Our findings suggest that encountering parasites affects migratory activity, regardless of whether infection occurs or is resisted.

Migration Takes Extra Guts for Juvenile Songbirds: Energetics and Digestive Physiology During the First Journey

Many birds undertake long migrations when they are only a few months of age. Although they are typically of adult body size, their performance and survival are often poor compared to adults. This differential performance could be due to lack of experience, selection against poor-performing cohort members, or inherent constraints of continuing physiological and morphological maturation of juveniles. Limited evidence suggests that digestive and muscle physiology of juveniles during their first migration may differ from that of adults. We compared body composition, metabolic rate, and digestive physiology between juvenile and adult passerines during fall migration. First, we measured fat and lean masses by quantitative magnetic resonance, and organ and muscle masses of salvaged carcasses of fall migrants from four passerine species. In general, juveniles had more lean mass and heavier digestive organs (especially liver) than adults in hermit thrushes (Catharus guttatus), Swainson’s thrushes (Catharus ustulatus), ovenbirds (Seiurus aurocapilla), and white-throated sparrows (Zonotrichia albicollis). Principal components analysis of all organs and muscles revealed that juveniles for three of four species had overall larger digestive components and smaller flight muscles than adults. We then used open-flow respirometry to measure basal metabolic rates (BMRs) of juvenile and adult Swainson’s thrushes and white-throated sparrows captured in fall at a migratory stopover site. Controlling for a significant effect of body mass, juveniles had 6% higher BMRs than adults in both species. We then conducted total collection mass balance feeding trials with fall migratory Swainson’s thrushes and white-throated sparrows. Juvenile thrushes had greater metabolizable energy intake than adults, which was achieved through higher food intake rather than greater utilization efficiency. Age classes of white-throated sparrows did not differ in these measures of digestive performance, although juveniles had greater food intake capacity at low lean body masses. We propose that age-related differences in foraging ecology, diet composition and energy requirements may be responsible for larger digestive organs of juvenile migrants. Larger guts may allow juveniles to consume more food or a more dilute diet, but may contribute to higher BMRs.

Regional epigenetic differentiation of the Z Chromosome between sexes in a female heterogametic system.

In male heterogametic systems, the X Chromosome is epigenetically differentiated between males and females, to facilitate dosage compensation. For example, the X Chromosome in female mammals is largely inactivated. Relative to well-studied male heterogametic systems, the extent of epigenetic differentiation between male and female Z Chromosomes in female heterogametic species, which often lack complete dosage compensation, is poorly understood. Here, we examined the chromosomal DNA methylation landscapes of male and female Z Chromosomes in two distantly related avian species, namely chicken and white-throated sparrow. We show that, in contrast to the pattern in mammals, male and female Z Chromosomes in these species exhibit highly similar patterns of DNA methylation, which is consistent with weak or absent dosage compensation. We further demonstrate that the epigenetic differences between male and female chicken Z Chromosomes are localized to a few regions, including a previously identified male hypermethylated region 1 (MHM1; CGNC: 80601). We discovered a novel region with elevated male-to-female methylation ratios on the chicken Z Chromosome (male hypermethylated region 2 [MHM2]; CGNC: 80602). The MHM1 and MHM2, despite little sequence similarity between them, bear similar molecular features that are likely associated with their functions. We present evidence consistent with female hypomethylation of MHMs and up-regulation of nearby genes. Therefore, despite little methylation differentiation between sexes, extremely localized DNA methylation differences between male and female chicken Z Chromosomes have evolved and affect expression of nearby regions. Our findings offer new insights into epigenetic regulation of gene expression between sexes in female heterogametic systems.

Parent and offspring genotypes influence gene expression in early life.

Parents can have profound effects on offspring fitness. Little, however, is known about the mechanisms through which parental genetic variation influences offspring physiology in natural systems. White-throated sparrows (Zonotrichia albicollis, WTSP) exist in two genetic morphs, tan and white, controlled by a large polymorphic supergene. Morphs mate disassortatively, resulting in two pair types: tan male×white female (T×W) pairs, which provide biparental care and white male×tan female (W×T) pairs, which provide female-biased care. To investigate how parental composition impacts offspring, we performed RNA-seq on whole blood of WTSP nestlings sampled from nests of both pair types. Parental pair type had a large effect on nestling gene expression, with 881 genes differentially expressed (DE) and seven correlated gene coexpression modules. The DE genes and modules expressed at higher levels in W×T nests with female-biased parental care function in metabolism and stress-related pathways resulting from the overrepresentation of proteolysis and stress-response genes (e.g., SOD2, NR3C1). These results show that parental genotypes and/or associated behaviours influence nestling physiology, and highlight avenues of further research investigating the ultimate implications for the maintenance of this polymorphism. Nestlings also exhibited morph-specific gene expression, with 92 differentially expressed genes, comprising immunity genes and genes encompassed by the supergene. Remarkably, we identified the same regulatory hub genes in these blood-derived expression networks as were previously identified in adult WTSP brains (EPM2A, BPNT1, TAF5L). These hub genes were located within the supergene, highlighting the importance of this gene complex in structuring regulatory networks across diverse tissues.

Experimental traffic noise attracts birds during the breeding season

Abstract Understanding how anthropogenic disturbance affects animal behavior is challenging because observational studies often involve co-occurring disturbances (e.g., noise, lighting, and roadways), and laboratory experiments often lack ecological validity. During the 2016 and 2017 avian breeding seasons, we investigated the effects of anthropogenic noise and light on the singing and spatial behavior of wild birds by independently manipulating the presence of each type of disturbance at 89 sites in an otherwise undisturbed boreal forest in Labrador, Canada. Each treatment was surrounded by an eight-channel microphone array that recorded and localized avian vocalizations throughout the manipulation. We analyzed the effects of noise and light on the timing of the first vocalizations of each species at each array during the dawn chorus, and on the proximity of the vocalizing birds to the disturbance when those songs were produced. We analyzed all species combined, and then conducted separate analyses for the six most common species: boreal chickadee, dark-eyed junco, ruby-crowned kinglet, Swainson’s thrush, white-throated sparrow, and yellow-rumped warbler. When all species were analyzed together, we found that traffic noise attracted vocalizing birds. There was some evidence that light repelled birds, but this evidence was inconsistent. In our species-specific analyses, yellow-rumped warbler sang earlier in response to noise; Swainson’s thrush was attracted to noise and the combination of noise and light but repelled by light alone. Our study provides some of the first experimental evidence of the independent and combined effects of traffic noise and light on the vocal and spatial behavior of wild birds and suggests that breeding birds may be attracted to noisy roads where they could be exposed to additional forms of disturbance.

New avian breeding records for Kugluktuk, Nunavut

New breeding records for 10 species of tundra and boreal nesting birds were documented near the community of Kugluktuk (Nunavut, Canada) over the course of the 2015 and 2016 breeding seasons and incidentally in 2017 and 2018. These species include American Wigeon (Mareca americana), Mallard (Anas platyrhynchos), Northern Shoveler (Anas clypeata), Green-winged Teal (Anas carolinensis), Greater Scaup (Aythya marila), Say’s Phoebe (Sayornis saya), Canada Jay (Perisoreus canadensis), Greycheeked Thrush (Catharus minimus), Yellow-rumped Warbler (Setophaga coronata), and Dark-eyed Junco (Junco hyemalis). Previously unpublished breeding evidence for Bald Eagle (Haliaeetus leucocephalus) is also discussed along with suspected breeding of Barn Swallow (Hirundo rustica), Bohemian Waxwing (Bombycilla garrulus), White-throated Sparrow (Zonotrichia albicollis), and Pine Grosbeak (Pinicola enucleator). These records represent the first described breeding occurrences for these species in the Kitikmeot region, or new records for the mainland of Nunavut. A lack of historical ornithological survey effort in this area has likely led to the diversity of these previously unrecorded breeding observations. These results highlight the need to increase geographic coverage of bird surveys in northern Canada to more accurately delineate the northern limit of breeding ranges and suggest that further formal survey effort will undoubtedly lead to additional new breeding records.

Extrapair mating and the strength of sexual selection: insights from a polymorphic species.

Extrapair mating could drive sexual selection in socially monogamous species, but support for this hypothesis remains equivocal. We used lifetime fitness data and a unique model species, the dimorphic white-throated sparrow (Zonotrichia albicollis), to examine how extrapair mating affects the potential for sexual selection. In this species, the morphs employ distinct reproductive strategies, with white males pursuing extrapair mating at higher rates than tan counterparts. Social and extrapair mating is disassortative by morph, with paternity exchange occurring primarily between pairs composed of white males and tan females. Bateman gradients and Jones indexes indicated stronger sexual selection via mate numbers in white males than in females and tan males, and generally did not differ between females as compared with tan males. Extrapair mating contributed more to the Bateman gradient for white than tan males, and white males also had higher variance in annual reproductive success. However, variance in lifetime reproductive success did not differ between morphs or sexes. Moreover, extrapair mating did not increase variance in male reproductive success relative to apparent patterns, and within-pair success accounted for much more variance than extrapair success. Thus, extrapair mating by white males increases Bateman gradients and the potential for sexual selection via mate numbers. However, our latter results support previous research suggesting that extrapair mating may play a limited role in driving the overall potential for sexual selection.

Influence of the Agricultural Conservation Easement Program wetland practices on winter occupancy of Passerellidae sparrows and avian species richness.

Wetlands enrolled in the Agricultural Conservation Easement Program (ACEP) are established as a means of restoring wetland ecosystems and wildlife habitat on private, agricultural land. In West Virginia, USA, ACEP wetlands have never been evaluated to determine how they function as wildlife habitat in comparison to other available wetland habitat in the state. We measured the wintering occupancy of Passerellidae species and apparent avian species richness on ACEP wetlands and a set of reference wetlands located on public land in West Virginia to evaluate if ACEP wetlands are being used similarly by avian species to other available wetland habitat in the state. Apparent avian species richness and the occupancy probability of four Passerellidae species—song sparrows (Melospiza melodia), dark-eyed juncos (Junco hyemalis), swamp sparrows (Melospiza georgiana), and white-throated sparrows (Zonotrichia albicollis)—did not differ between ACEP and reference sites. In addition to other vegetative and habitat associations for each species, dark-eyed junco occupancy was negatively correlated with wetland size while swamp sparrow occupancy and apparent avian species richness were positively associated with wetland size. These results indicate that ACEP wetlands are providing winter avian habitat as well as another source of wetland habitat in the state. Maintaining and expanding ACEP wetlands in West Virginia would continue to provide wetland systems in areas that are otherwise lacking these habitats.

Actuarial senescence in a dimorphic bird: different rates of ageing in morphs with discrete reproductive strategies.

It is often hypothesized that intra-sexual competition accelerates actuarial senescence, or the increase in mortality rates with age. However, an alternative hypothesis is that parental investment is more important to determining senescence rates. We used a unique model system, the white-throated sparrow (Zonotrichia albicollis), to study variation in actuarial senescence. In this species, genetically determined morphs display discrete mating strategies and disassortative pairing, providing an excellent opportunity to test the predictions of the above hypotheses. Compared to tan-striped males, white-striped males are more polygynous and aggressive, and less parental. Tan-striped females receive less parental support, and invest more into parental care than white-striped females, which are also more aggressive. Thus, higher senescence rates in males and white-striped birds would support the intra-sexual competition hypothesis, whereas higher senescence rates in females and tan-striped birds would support the parental investment hypothesis. White-striped males showed the lowest rate of actuarial senescence. Tan-striped females had the highest senescence rate, and tan-striped males and white-striped females showed intermediate, relatively equal rates. Thus, results were inconsistent with sexual selection and competitive strategies increasing senescence rates, and instead indicate that senescence may be accelerated by female-biased parental care, and lessened by sharing of parental duties.

Developmental stress and telomere dynamics in a genetically polymorphic species.

A central objective of evolutionary biology is understanding variation in life-history trajectories and the rate of aging, or senescence. Senescence can be affected by trade-offs and behavioural strategies in adults but may also be affected by developmental stress. Developmental stress can accelerate telomere degradation, with long-term longevity and fitness consequences. Little is known regarding whether variation in developmental stress and telomere dynamics contributes to patterns of senescence during adulthood. We investigated this question in the dimorphic white-throated sparrow (Zonotrichia albicollis), a species in which adults of the two morphs exhibit established differences in behavioural strategy and patterns of senescence, and also evaluated the relationship between oxidative stress and telomere length. Tan morph females, which exhibit high levels of unassisted parental care, display faster reproductive senescence than white females, and faster actuarial senescence than all of the other morph-sex classes. We hypothesized that high oxidative stress and telomere attrition in tan female nestlings could contribute to this pattern, since tan females are small and potentially at a competitive disadvantage even as nestlings. Nestlings that were smaller than nest mates had higher oxidative stress, and nestlings with high oxidative stress and fast growth rates displayed shorter telomeres. However, we found no consistent morph-sex differences in oxidative stress or telomere length. Results suggest that oxidative stress and fast growth contribute to developmental telomere attrition, with potential ramifications for adults, but that developmental oxidative stress and telomere dynamics do not account for morph-sex differences in senescence during adulthood.

Spatial variation in White-throated Sparrow (Zonotrichia albicollis) refueling rate near a migratory barrier

ABSTRACT Stopover sites are essential to bird migration between wintering and breeding grounds, but annual variation in use and habitat conditions make it difficult to determine which sites are mos...

Spatial variation in White-throated Sparrow (Zonotrichia albicollis) refueling rate near a migratory barrier

Spatial variation in White-throated Sparrow (Zonotrichia albicollis) refueling rate near a migratory barrier

Alternative reproductive strategies in white-throated sparrows are associated with differences in parasite load following experimental infection.

Immune defences often trade off with other life-history components. Within species, optimal allocation to immunity may differ between the sexes or between alternative life-history strategies. White-throated sparrows (Zonotrichia albicollis) are unusual in having two discrete plumage morphs, white-striped and tan-striped. Within each sex, white-striped individuals are more aggressive and provide less parental care than tan-striped individuals. We extended immunocompetence handicap models, which predict sex differences in immunity and parasitism, to hypothesize that infection susceptibility should be greater in white-striped than tan-striped birds. We inoculated birds of both morphs with malarial parasites. Contrary to our prediction, among birds that became infected, parasite loads were higher in tan-striped than white-striped individuals and did not differ between the sexes. Circulating androgen levels did not differ between morphs but were higher in males than females. Our findings are not consistent with androgen-mediated immunosuppression. Instead, morph differences in immunity could reflect social interactions or life-history-related differences in risk of injury, and/or genetic factors. Although plumage and behavioural morphs of white-throated sparrow may differ in disease resistance, these differences do not parallel sex differences that have been reported in animals, and do not appear to be mediated by differences in androgen levels.