Phylogenetic Analysis of Buggy Creek Virus: Evidence for Multiple Clades in the Western Great Plains, United States of America

We present the first detailed phylogenetic analysis of Buggy Creek virus (BCRV), a poorly known alphavirus with transmission cycles involving a cimicid swallow bug (Oeciacus vicarius) vector and cliff swallows (Petrochelidon pyrrhonota) and house sparrows (Passer domesticus) as the principal avian hosts. Nucleotide sequences of a 2,075-bp viral envelope glycoprotein-coding region, covering the entire PE2 gene, were determined for 33 BCRV isolates taken from swallow bugs at cliff swallow colonies in Nebraska and Colorado in the summer of 2001 and were compared with the corresponding region of BCRV isolates collected from Oklahoma in the 1980s. We also analyzed isolates of the closely related Fort Morgan virus (FMV) collected from Colorado in the 1970s. Phylogenetic analysis indicated that BCRV falls into the western equine encephalomyelitis complex of alphaviruses, in agreement with antigenic results and a previous alphavirus phylogeny based on the E1 coding region. We found four distinct BCRV/FMV clades, one each unique to Nebraska, Colorado, and Oklahoma and one containing isolates from both Nebraska and Colorado. BCRV isolates within the two clades from Nebraska showed 5.7 to 6.2% nucleotide divergence and 0.7 to 1.9% amino acid divergence, and within these clades, we found multiple subclades. Nebraska subclades tended to be confined to one or a few cliff swallow colonies that were close to each other in space, although in some cases, near-identical isolates were detected at sites up to 123 km apart. Viral gene flow occurs when cliff swallows move (bugs) between colony sites, and the genetic structure of BCRV may reflect the limited dispersal abilities of its insect vector.     

Predation by ants controls swallow bug (Hemiptera: Cimicidae: Oeciacus vicarius) infestations

The swallow bug (Oeciacus vicarius) is the only known vector for Buggy Creek virus (BCRV), an alphavirus that circulates in cliff swallows (Petrochelidon pyrrhonota) and house sparrows (Passer domesticus) in North America. We discovered ants (Crematogaster lineolata and Formica spp.) preying on swallow bugs at cliff swallow colonies in western Nebraska, U.S.A. Ants reduced the numbers of visible bugs on active swallow nests by 74‐90%, relative to nests in the same colony without ants. Ant predation on bugs had no effect on the reproductive success of cliff swallows inhabiting the nests where ants foraged. Ants represent an effective and presumably benign way of controlling swallow bugs at nests in some colonies. They may constitute an alternative to insecticide use at sites where ecologists wish to remove the effects of swallow bugs on cliff swallows or house sparrows. By reducing bug numbers, ant presence may also lessen BCRV transmission at the spatial foci (bird colony sites) where epizootics occur. The effect of ants on swallow bugs should be accounted for in studying variation among sites in vector abundance.     

An enzootic vector-borne virus is amplified at epizootic levels by an invasive avian host

Determining the effect of an invasive species on enzootic pathogen dynamics is critical for understanding both human epidemics and wildlife epizootics. Theoretical models suggest that when a naive species enters an established host–parasite system, the new host may either reduce (‘dilute’) or increase (‘spillback’) pathogen transmission to native hosts. There are few empirical data to evaluate these possibilities, especially for animal pathogens. Buggy Creek virus (BCRV) is an arthropod-borne alphavirus that is enzootically transmitted by the swallow bug (Oeciacus vicarius) to colonially nesting cliff swallows (Petrochelidon pyrrhonota). In western Nebraska, introduced house sparrows (Passer domesticus) invaded cliff swallow colonies approximately 40 years ago and were exposed to BCRV. We evaluated how the addition of house sparrows to this host–parasite system affected the prevalence and amplification of a bird-associated BCRV lineage. The infection prevalence in house sparrows was eight times that of cliff swallows. Nestling house sparrows in mixed-species colonies were significantly less likely to be infected than sparrows in single-species colonies. Infected house sparrows circulated BCRV at higher viraemia titres than cliff swallows. BCRV detected in bug vectors at a site was positively associated with virus prevalence in house sparrows but not with virus prevalence in cliff swallows. The addition of a highly susceptible invasive host species has led to perennial BCRV epizootics at cliff swallow colony sites. The native cliff swallow host confers a dilution advantage to invasive sparrow hosts in mixed colonies, while at the same sites house sparrows may increase the likelihood that swallows become infected.     

Arbovirus infection increases with group size

Buggy Creek (BCR) virus is an arthropod-borne alphavirus that is naturally transmitted to its vertebrate host the cliff swallow (Petrochelidon pyrrhonota) by an invertebrate vector, namely the cimicid swallow bug (Oeciacus vicarius). We examined how the prevalence of the virus varied with the group size of both its vector and host. The study was conducted in southwestern Nebraska where cliff swallows breed in colonies ranging from one to 3700 nests and the bug populations at a site vary directly with the cliff swallow colony size. The percentage of cliff swallow nests containing bugs infected with BCR virus increased significantly with colony size at a site in the current year and at the site in the previous year. This result could not be explained by differences in the bug sampling methods, date of sampling, sample size of the bugs, age structure of the bugs or the presence of an alternate host, the house sparrow (Passer domesticus). Colony sites that were reused by cliff swallows showed a positive autocorrelation in the percentage of nests with infected bugs between year t and year t+1, but the spatial autocorrelation broke down for year t+2. The increased prevalence of BCR virus at larger cliff swallow colonies probably reflects the larger bug populations there, which are less likely to decline in size and lead to virus extinction. To the authors' knowledge this is the first demonstration of arbovirus infection increasing with group size and one of the few known predictive ecological relationships between an arbovirus and its vectors/hosts. The results have implications for both understanding the fitness consequences of coloniality for cliff swallows and understanding the temporal and spatial variation in arboviral epidemics.     

Isolation by distance explains genetic structure of Buggy Creek virus,a bird-associated arbovirus

Many of the arthropod-borne viruses (arboviruses) show extensive genetic variability and are widely distributed over large geographic areas. Understanding how virus genetic structure varies in space may yield insight into how these pathogens are adapted to and dispersed by different hosts or vectors, the relative importance of mutation, drift, or selection in generating genetic variability, and where and when epidemics or epizootics are most likely to occur. However, because most arboviruses tend to be sampled opportunistically and often cannot be isolated in large numbers at a given locale, surprisingly little is known about their spatial genetic structure on the local scale at which host/vector/virus interactions typically occur. Here, we examine fine-scale spatial structure of two sympatric lineages of Buggy Creek virus (BCRV, Togaviridae), an alphavirus transmitted by the ectoparasitic swallow bug (Oeciacus vicarius) to colonially nesting cliff swallows (Petrochelidon pyrrhonota) and invasive house sparrows (Passer domesticus) in North America. Data from 377 BCRV isolates at cliff swallow colony sites in western Nebraska showed that both virus lineages were geographically structured. Most haplotypes were detected at a single colony or were shared among nearby colonies, and pair-wise genetic distance increased significantly with geographic distance between colony sites. Genetic structure of both lineages is consistent with isolation by distance. Sites with the most genetically distinct BCRV isolates were occupied by large numbers of house sparrows, suggesting that concentrations of invasive sparrows may represent foci for evolutionary change in BCRV. Our results show that bird-associated arboviruses can show genetic substructure over short geographic distances.     

Group size and nest spacing affect Buggy Creek virus (Togaviridae: Alphavirus) infection in nestling house sparrows

The transmission of parasites and pathogens among vertebrates often depends on host population size, host species diversity, and the extent of crowding among potential hosts, but little is known about how these variables apply to most vector-borne pathogens such as the arboviruses (arthropod-borne viruses). Buggy Creek virus (BCRV; Togaviridae: Alphavirus) is an RNA arbovirus transmitted by the swallow bug (Oeciacus vicarius) to the cliff swallow (Petrochelidon pyrrhonota) and the introduced house sparrow (Passer domesticus) that has recently invaded swallow nesting colonies. The virus has little impact on cliff swallows, but house sparrows are seriously affected by BCRV. For house sparrows occupying swallow nesting colonies in western Nebraska, USA, the prevalence of BCRV in nestling sparrows increased with sparrow colony size at a site but decreased with the number of cliff swallows present. If one nestling in a nest was infected with the virus, there was a greater likelihood that one or more of its nest-mates would also be infected than nestlings chosen at random. The closer a nest was to another nest containing infected nestlings, the greater the likelihood that some of the nestlings in the focal nest would be BCRV-positive. These results illustrate that BCRV represents a cost of coloniality for a vertebrate host (the house sparrow), perhaps the first such demonstration for an arbovirus, and that virus infection is spatially clustered within nests and within colonies. The decreased incidence of BCRV in sparrows as cliff swallows at a site increased reflects the "dilution effect," in which virus transmission is reduced when a vector switches to feeding on a less competent vertebrate host.     

Immune Responses of a Native and an Invasive Bird to Buggy Creek Virus (Togaviridae: Alphavirus) and Its Arthropod Vector,the Swallow Bug (Oeciacus vicarius)

Invasive species often display different patterns of parasite burden and virulence compared to their native counterparts. These differences may be the result of variability in host-parasite co-evolutionary relationships, the occurrence of novel host-parasite encounters, or possibly innate differences in physiological responses to infection between invasive and native hosts. Here we examine the adaptive, humoral immune responses of a resistant, native bird and a susceptible, invasive bird to an arbovirus (Buggy Creek virus; Togaviridae: Alphavirus) and its ectoparasitic arthropod vector (the swallow bug; Oeciacus vicarius). Swallow bugs parasitize the native, colonially nesting cliff swallow (Petrochelidon pyrrhonota) and the introduced house sparrow (Passer domesticus) that occupies nests in cliff swallow colonies. We measured levels of BCRV-specific and swallow bug-specific IgY levels before nesting (prior to swallow bug exposure) and after nesting (after swallow bug exposure) in house sparrows and cliff swallows in western Nebraska. Levels of BCRV-specific IgY increased significantly following nesting in the house sparrow but not in the cliff swallow. Additionally, house sparrows displayed consistently higher levels of swallow bug-specific antibodies both before and after nesting compared to cliff swallows. The higher levels of BCRV and swallow bug specific antibodies detected in house sparrows may be reflective of significant differences in both antiviral and anti-ectoparasite immune responses that exist between these two avian species. To our knowledge, this is the first study to compare the macro- and microparasite-specific immune responses of an invasive and a native avian host exposed to the same parasites.     

The incidence of American swallow bugs (Oeciacus vicarius) in barn swallow (Hirundo rustica) colonies in northeast Texas

The American swallow bug (Oeciacus vicarius) is an important ectoparasite of cliff swallows (Petrochelidon pyrrhonota) and is known to harbor several types of arbovirus. A recent study in northeast Texas suggested that O. vicarius might occur in barn swallows (Hirundo rustica) at rates much higher than previously thought. The purpose of this study was to determine the extent to which barn swallows in northeast Texas are parasitized by O. vicarius and how well this parasite is adapting to this novel host. A sample of 498 nests at 54 colonies was inspected for O. vicarius. Forty colonies (74.1%) were infected, while 310 nests (62.2%) were infected. Large colonies were more likely to be infected than small colonies. Colonies that also contained cliff swallows were more likely to be infected than colonies without cliff swallows. Infection levels in barn swallow nests were comparable to those reported for cliff swallows, though age and sex class ratios differed. Demographic changes among swallow species, including range expansions, increased colony sizes, and more frequent interspecific nesting associations have likely facilitated the movement of O. vicarius from the cliff swallow into a novel host, the barn swallow.     

Between-group transmission dynamics of the swallow bug, Oeciacus vicarius.

The parasitic cimicid swallow bug, Oeciacus vicarius, is the principal invertebrate vector for Buggy Creek virus (BCRV) and has also been associated with Venezuelan equine encephalitis virus. To help understand the spread of this vector, we experimentally measured the transmission of O. vicarius between groups (colonies) of its main host, the cliff swallow (Petrochelidonpyrrhonota), in the field. Transmission of bugs between colonies varied significantly with year, size of the colony, and week within the season. Bug immigration into sites tended to peak in mid-summer. Swallow nests in larger colonies had more consistent rates of bug introduction than did nests in small colonies, but within a colony a given nest's weekly immigrant-bug count varied widely across the season. Transmission of O. vicarius between host social groups follows broadly predictable seasonal patterns, but there is nevertheless temporal and spatial heterogeneity in bug transmission. By understanding how long-distance movement by this vector varies in time and space, we can better predict where and when BCRV epizootics may occur.     

Seasonal variation and age-related correlates of Buggy Creek virus (Togaviridae) infection in nestling house sparrows

Wild birds are rarely found with active arbovirus infections, and relatively little is known about the patterns of viremia they exhibit under field conditions or how infection varies with date, bird age, or other factors that potentially affect transmission dynamics. Buggy Creek virus (BCRV; Togaviridae, Alphavirus) is an arbovirus associated with colonially nesting Cliff Swallows (Petrochelidon pyrrhonota) and transmitted by its vector, the hematophagous swallow bug (Oeciacus vicarius), an ectoparasite of the Cliff Swallow. Introduced House Sparrows (Passer domesticus) that have occupied swallow nests at colony sites in peridomestic settings are also exposed to BCRV when fed upon by swallow bugs. We used data from 882 nestling House Sparrows in western Nebraska from 2006 to 2008 to examine seasonal variation and age-related correlates of virus infection in the field. Over 17% of nestling House Sparrows had active infections. Prevalence was higher in 2007 than in 2008 when birds from all colony sites were analyzed, but there was no significant difference between years for sites sampled in both seasons. Buggy Creek virus prevalence was similar in early and late summer, with a peak in midsummer, coinciding with the greatest swallow bug abundance. Nestlings 10 days of age and younger were most commonly infected, and the likelihood of BCRV infection declined for older nestlings. Average viremia titers also declined with age (but did not vary with date) and were high enough at all nestling ages to likely infect blood-feeding arthropods (swallow bugs). Length of viremia for nestlings in the field was ≥4 days, in agreement with an earlier study of BCRV. Nestling birds offer many advantages for field studies of arbovirus amplification and transmission.     

Host and vector movement affects genetic diversity and spatial structure of Buggy Creek virus (Togaviridae)

Determining the degree of genetic variability and spatial structure of arthropod-borne viruses (arboviruses) may help in identifying where strains that potentially cause epidemics or epizootics occur. Genetic diversity in arboviruses is assumed to reflect relative mobility of their vertebrate hosts (and invertebrate vectors), with highly mobile hosts such as birds leading to genetic similarity of viruses over large areas. There are no empirical studies that have directly related host or vector movement to virus genetic diversity and spatial structure. Using the entire E2 glycoprotein-coding region of 377 Buggy Creek virus isolates taken from cimicid swallow bugs (Oeciacus vicarius), the principal invertebrate vector for this virus, we show that genetic diversity between sampling sites could be predicted by the extent of movement by transient cliff swallows (Petrochelidon pyrrhonota) between nesting colonies where the virus and vectors occur. Pairwise F(ST) values between colony sites declined significantly with increasing likelihood of a swallow moving between those sites per 2-day interval during the summer nesting season. Sites with more bird movement between them had virus more similar genetically than did pairs of sites with limited or no bird movement. For one virus lineage, Buggy Creek virus showed greater haplotype and nucleotide diversity at sites that had high probabilities of birds moving into or through them during the summer; these sites likely accumulated haplotypes by virtue of frequent virus introductions by birds. Cliff swallows probably move Buggy Creek virus by transporting infected bugs on their feet. The results provide the first empirical demonstration that genetic structure of an arbovirus is strongly associated with host/vector movement, and suggest caution in assuming that bird-dispersed arboviruses always have low genetic differentiation across different sites.     

Dispersing hemipteran vectors have reduced arbovirus prevalence

A challenge in managing vector-borne zoonotic diseases in human and wildlife populations is predicting where epidemics or epizootics are likely to occur, and this requires knowing in part the likelihood of infected insect vectors dispersing pathogens from existing infection foci to novel areas. We measured prevalence of an arbovirus, Buggy Creek virus, in dispersing and resident individuals of its exclusive vector, the ectoparasitic swallow bug (Oeciacus vicarius), that occupies cliff swallow (Petrochelidon pyrrhonota) colonies in western Nebraska. Bugs colonizing new colony sites and immigrating into established colonies by clinging to the swallows’ legs and feet had significantly lower virus prevalence than bugs in established colonies and those that were clustering in established colonies before dispersing. The reduced likelihood of infected bugs dispersing to new colony sites indicates that even heavily infected sites may not always export virus to nearby foci at a high rate. Infected arthropods should not be assumed to exhibit the same dispersal or movement behaviour as uninfected individuals, and these differences in dispersal should perhaps be considered in the epidemiology of vector-borne pathogens such as arboviruses.     

Ectoparasites cause increased bilateral asymmetry of naturally selected traits in a colonial bird

Abstract Parasitism has been shown to correlate with levels of bilateral symmetry in some organisms, with more asymmetric individuals often having more parasites. However, few studies have shown experimentally that parasitism directly causes increased asymmetry. By fumigating some cliff swallow (Petrochelidon pyrrhonota) colonies and leaving others untreated, we investigated experimentally whether ectoparasitism by the cimicid swallow bug led to higher levels of asymmetry in length of wings, outer tail feathers, and tarsus among juvenile and adult birds. Juveniles from fumigated colonies measured soon after fledging had significantly less asymmetry in wing and outer tail length than juveniles from nonfumigated colonies; asymmetry in tarsus length was unaffected by parasitism. Adults that had undergone one or more post‐juvenal molts on the wintering grounds showed no differences in asymmetry between those reared in fumigated vs. nonfumigated colonies. These results show that ectoparasitism directly leads to increased feather asymmetry in cliff swallows, probably through parasite‐induced nutritional stress. Because wing and tail asymmetry impair flight performance and reduce foraging efficiency, the increased asymmetry caused by parasites represents a fitness cost to cliff swallows. This is among the few experimental studies to show an effect of parasites on asymmetry of naturally selected characters.     

Negative indirect effects of an avian insectivore on the fruit set of an insect-pollinated herb

Though an abundance of research has focused on direct interactions between birds and plants, relatively few studies have reported on indirect interactions. Of those reports, all have focused on positive indirect effects of birds on plants through predation of plant natural enemies. We conducted an observational study along the Middle Rio Grande in New Mexico to determine if avian aerial insectivores had a negative, indirect impact on insect-pollinated plants through predation of insect pollinators. We found considerable taxonomic overlap, at the order and family level, between insects visiting sweet clover ( Melilotus officinalis ) and those eaten by cliff swallows ( Hirundo pyrrhonota ). We found a significant negative relationship between proximity of sweet clover to cliff swallow breeding colonies and sweet clover fruit set during the cliff swallow nestling period. The apparent effect of cliff swallows was strongest within 200 m of breeding colonies (approximately 50% reduction in fruit set) and decreased nonlinearly to a distance of approximately 400 m. Finally, we found that the clover fruit set gradient disappeared after the nestling period, when chicks had fledged and the colony was abandoned.     

Barn swallows before barns: population histories and intercontinental colonization

The barn swallow (Hirundo rustica) is one of most widely distributed swallows, owing in part to its recent switch from natural nest sites to human structures. We conducted phylogenetic analysis of mitochondrial (mt) and nuclear DNA to explore the recent evolutionary history of this species. Strongly supported mtDNA clades corresponded to Europe, Asia and North America plus the Baikal region of Asia. Analysis of sequence data from a sex-linked nuclear gene was unable to recover the phylogenetic splits in the mtDNA tree, confirming that the main clades evolved recently. The phylogenetic pattern suggests that the ancestral area of the barn swallow was the holarctic; most divergence events are consistent with vicariance. Most unexpectedly, analyses show that barn swallows from North America colonized the Baikal region in the recent past (one fixed substitution). This dispersal direction is opposite of that for most nearctic-palearctic taxon exchanges. Although this invasion was envisioned to coincide with the appearance of new types of human dwelling in the Baikal region, calibration of molecular divergence suggests an older dispersal event. A recent history of gene flow within the main palearctic clades is consistent with range and population expansion owing to new nesting opportunities provided by human settlements. Contrary to expectation, populations in North America appear historically larger and more stable than those in the palearctic. The Baikal population apparently has not increased greatly since colonization.     

Variation in age composition among colony sizes in Cliff Swallows

Variation in group size is characteristic of most social species. The extent to which individuals sort among group sizes based on age may yield insight into why groups vary in size and the age‐specific costs and benefits of different social environments. We investigated the age composition of Cliff Swallow (Petrochelidon pyrrhonota) colonies of different sizes over 18 yr at a long‐term study site in western Nebraska, USA. Using years elapsed since banding as a relative measure of age for over 194,000 birds, we found that the proportion of age‐class‐1 swallows (birds banded as nestlings or juveniles or adults in the year of banding) of both sexes increased in larger colonies and at colony sites becoming active later in the summer. Age composition was unrelated to how often a particular colony site was used. The effect of colony size most likely reflected the fact that older birds return to the same colony site in successive years even when the colony size there decreases, and that yearlings and immigrants benefit more from larger colonies than do older, more experienced individuals. The date effect probably resulted in part from later spring arrival by younger and/or immigrant swallows. At fumigated sites where ectoparasitic swallow bugs (Oeciacus vicarius) had been removed, age composition did not vary with either colony size or colony initiation date. The patterns reported here appear to be driven partially by the presence of ectoparasites and suggest that the hematophagous bugs influence variation in Cliff Swallow group composition. Our results are consistent with the hypothesis that variation in colony size reflects, in part, age‐based sorting of individuals among groups.     

Parent-offspring recognition in the barn swallow (Hirundo rustica)

Past research has shown that in the colonial bank swallow and cliff swallow, parents and offspring recognize one another by calls, enabling parents to locate and feed only their own chicks. To test the hypothesis that recognition traits are adaptations to coloniality, we examined parent-offspring recognition in the related but non-colonial species, the barn swallow. To allow cross-species comparisons, we used the same methods that had been used in the previous swallow studies. We carried out four studies. (1) Cross-fostering experiments done immediately before fledging gave no evidence of recognition. (2) In a playback experiment, parents gave no indication that they recognized the calls of their offspring. (3) In another playback experiment, chicks responded more strongly to the calls of their parents than to the calls of unrelated adults. The degree of recognition, however, was somewhat weaker than that seen in the two colonial swallow species. (4) Newly fledged young did not creche after fledging. Rather, family groups generally stayed apart from one another for almost 2 weeks, while parental care was still being given. The comparative data suggest that parent-offspring recognition via individually distinctive cues evolved in response to the intermingling of young associated with colonial living, and it thus weakly expressed in barn swallows compared to cliff swallows and bank swallows.     

Nest spacing in relation to settlement time in colonial cliff swallows

How colonial animals space their nests in relation to conspecifics may provide clues as to whether coloniality provides net benefits or occurs only because breeding sites are limited. We examined how nearest-neighbour distance varied in relation to settlement time in the highly colonial cliff swallow, Petrochelidon pyrrhonota, comparing observed nearest-neighbour distances to those expected if birds spread out to maximize nest spacing. Cliff swallows generally settled closer to each other than required by the available substrate, and clustered their nests closer in large colonies than in small ones. The first settlers at a colony site spaced themselves further apart than later arrivals but did not maximize nearest-neighbour distances. The first arrivals maintained greater nest spacing throughout the season than did birds that arrived later. Colony size and amount of nesting substrate had no effect on initial settlement distances of the first arrivals, but eventual nearest-neighbour distances declined with colony size. First arrivals may gain less from nesting with conspecifics and thus are less likely to cluster their nests than later arrivals, which may often be young or na?ve birds that gain more from the social benefits of colonial nesting. The results are consistent with the presumed social advantages cliff swallows receive from coloniality and do not support the hypothesis that colonies result from nesting site limitation. Copyright 2000 The Association for the Study of Animal Behaviour.     

Heritable choice of colony size in cliff swallows: does experience trump genetics in older birds?

The variation in breeding-colony size seen in populations of most colonial birds may reflect heritable choices made by individuals who are phenotypically specialized for particular social environments. Although a few studies have reported evidence for genetically based choice of group sizes in birds, we know relatively little about the extent to which animals potentially rely on experience versus innate preferences in deciding with how many conspecifics to settle at different times of their lives. We conducted a cross-fostering experiment in 1997-1998 on cliff swallows (Petrochelidon pyrrhonota) in southwestern Nebraska, USA, in which some individuals were reared in colonies different in size from those in which they were born. Breeding-colony sizes chosen by this cohort of birds were monitored by mark-recapture throughout their lives. A multistate mark-recapture analysis revealed that birds in their first breeding year chose colony sizes similar to those of their birth, regardless of their rearing environment, confirming a previous analysis. Beyond the first breeding year, however, cliff swallows' colony choice was less dependent on where they were born. Birds born in small colonies and reared in large colonies showed evidence of a delayed rearing effect, with these birds overwhelmingly choosing large colonies in later years. Heritabilities suggested strong genetic effects on first-year colony choice but not in later years. Cliff swallows' genetically based colony-size preferences their first year could be a way to ensure matching of their phenotype to an appropriate social environment as yearlings. In later years, familiarity with particular colony sites and available information on site quality may override innate group-size preferences when birds choose colonies.