Limited genetic differentiation between acoustically divergent populations of urban and rural silvereyes (Zosterops lateralis)

The bioacoustic attributes of vocalisations made by birds in urban environments often differ markedly from those of rural conspecifics. Whether such differences are result from genetic divergence between urban and rural populations, or from plasticity or cultural evolution of song remains poorly understood. Silvereyes (Zosterops lateralis) show evidence of acoustic adaptation to urban noise, modifying both their songs and calls in cities when compared to rural areas. We investigated whether these differences were associated with corresponding morphological and neutral genetic differences. Across six pairs of geographically separate urban and rural populations, all morphological traits measured were similar. Furthermore, genetic analyses of variation at nine microsatellite loci revealed high levels of genetic connectivity between populations, and similar levels of heterozygosity in both habitat types. Consistent directional shifts in song attributes of city birds across large geographic areas thus do not appear to be accompanied by associated morphological or neutral genetic divergence.     

Independent colonization of multiple urban centres by a formerly forest specialist bird species

Urban areas are expanding rapidly, but a few native species have successfully colonized them. The processes underlying such colonization events are poorly understood. Using the blackbird Turdus merula, a former forest specialist that is now one of the most common urban birds in its range, we provide the first assessment of two contrasting urban colonization models. First, that urbanization occurred independently. Second, that following initial urbanization, urban-adapted individuals colonized other urban areas in a leapfrog manner. Previous analyses of spatial patterns in the timing of blackbird urbanization, and experimental introductions of urban and rural blackbirds to uncolonized cities, suggest that the leapfrog model is likely to apply. We found that, across the western Palaearctic, urban blackbird populations contain less genetic diversity than rural ones, urban populations are more strongly differentiated from each other than from rural populations and assignment tests support a rural source population for most urban individuals. In combination, these results provide much stronger support for the independent urbanization model than the leapfrog one. If the former model predominates, colonization of multiple urban centres will be particularly difficult when urbanization requires genetic adaptations, having implications for urban species diversity.     

The effect of urbanisation on avian morphology and latitudinal gradients in body size

Urban areas occupy a large and growing proportion of the earth. Such sites exhibit distinctive characteristics relative to adjacent rural habitats, and many species have colonised and now successfully exploit urban habitats. The change in selection pressures as a result of urbanisation has led to trait divergence in some urban populations relative to their rural counterparts, but studies have generally been local in scale and the generality of differentiation thus remains unknown. The European blackbird Turdus merula is one of the commonest urban bird species in the Western Palearctic, but populations vary substantially in the length of time they have been urbanised. Here we investigate patterns of morphological variation in European blackbirds occupying 11 paired urban and rural habitats across much of the urbanised range of this species and spanning 25° of latitude. First, we assessed the extent to which urban and rural blackbirds are differentiated morphologically and the consistency of any differentiation across the range. Paired urban and rural Blackbird populations frequently exhibited significant morphological differences, but the magnitude and direction of differentiation was site dependent. We then investigated whether the nature of latitudinal gradients in body‐size differed between urban and rural populations, as predicted by differences in the climatic regimes of urban and rural areas. Blackbird body‐size exhibited strong latitudinal gradients, but their form did not differ significantly between urban and rural habitats. The latitudinal gradient in body size may be a consequence of Seebohm's rule, that more migratory populations occurring at high latitudes have longer wings. We conclude that while there can be substantial morphological variation between adjacent urban and rural bird populations, such differentiation may not apply across a species’ range. Locality specific differentiation of urban and rural blackbirds may arise if the selection pressures acting on blackbird morphology vary in an inconsistent manner between urban and rural habitats. Alternatively, phenotypic divergence could arise in a stochastic manner depending on the morphological traits of colonists, through founder effects.     

Candidate gene polymorphisms for behavioural adaptations during urbanization in blackbirds

Successful urban colonization by formerly rural species represents an ideal situation in which to study adaptation to novel environments. We address this issue using candidate genes for behavioural traits that are expected to play a role in such colonization events. We identified and genotyped 16 polymorphisms in candidate genes for circadian rhythms, harm avoidance and migratory and exploratory behaviour in 12 paired urban and rural populations of the blackbird Turdus merula across the Western Palaearctic. An exonic microsatellite in the SERT gene, a candidate gene for harm avoidance behaviour, exhibited a highly significant association with habitat type in an analysis conducted across all populations. Genetic divergence at this locus was consistent in 10 of the 12 population pairs; this contrasts with previously reported stochastic genetic divergence between these populations at random markers. Our results indicate that behavioural traits related to harm avoidance and associated with the SERT polymorphism experience selection pressures during most blackbird urbanization events. These events thus appear to be influenced by homogeneous adaptive processes in addition to previously reported demographic founder events.     

Contrasting Patterns of Genetic Differentiation among Blackcaps (Sylvia atricapilla) with Divergent Migratory Orientations in Europe

Migratory divides are thought to facilitate behavioral, ecological, and genetic divergence among populations with different migratory routes. However, it is currently contentious how much genetic divergence is needed to maintain distinct migratory behavior across migratory divides. Here we investigate patterns of neutral genetic differentiation among Blackcap (Sylvia atricapilla) populations with different migratory strategies across Europe. We compare the level of genetic divergence of populations migrating to southwestern (SW) or southeastern (SE) wintering areas with birds wintering in the British Isles following a recently established northwesterly (NW) migration route. The migratory divide between SW and SE wintering areas can be interpreted as a result of a re-colonization process after the last glaciation. Thus we predicted greater levels of genetic differentiation among the SW/SE populations. However, a lack of genetic differentiation was found between SW and SE populations, suggesting that interbreeding likely occurs among Blackcaps with different migratory orientations across a large area; therefore the SW/SE migratory divide can be seen as diffuse, broad band and is, at best, a weak isolating barrier. Conversely, weak, albeit significant genetic differentiation was evident between NW and SW migrants breeding sympatrically in southern Germany, suggesting a stronger isolating mechanism may be acting in this population. Populations located within/near the SW/SE contact zone were the least genetically divergent from NW migrants, confirming NW migrants likely originated from within the contact zone. Significant isolation-by-distance was found among eastern Blackcap populations (i.e. SE migrants), but not among western populations (i.e. NW and SW migrants), revealing different patterns of genetic divergence among Blackcap populations in Europe. We discuss possible explanations for the genetic structure of European Blackcaps and how gene flow influences the persistence of divergent migratory behaviors.     

Settling down of seasonal migrants promotes bird diversification

How seasonal migration originated and impacted diversification in birds remains largely unknown. Although migratory behaviour is likely to affect bird diversification, previous studies have not detected any effect. Here, we infer ancestral migratory behaviour and the effect of seasonal migration on speciation and extinction dynamics using a complete bird tree of life. Our analyses infer that sedentary behaviour is ancestral, and that migratory behaviour evolved independently multiple times during the evolutionary history of birds. Speciation of a sedentary species into two sedentary daughter species is more frequent than speciation of a migratory species into two migratory daughter species. However, migratory species often diversify by generating a sedentary daughter species in addition to the ancestral migratory one. This leads to an overall higher migratory speciation rate. Migratory species also experience lower extinction rates. Hence, although migratory species represent a minority (18.5%) of all extant birds, they have a higher net diversification rate than sedentary species. These results suggest that the evolution of seasonal migration in birds has facilitated diversification through the divergence of migratory subpopulations that become sedentary, and illustrate asymmetrical diversification as a mechanism by which diversification rates are decoupled from species richness.     

Urbanization and its effects on personality traits: a result of microevolution or phenotypic plasticity?

Human‐altered environmental conditions affect many species at the global scale. An extreme form of anthropogenic alteration is the existence and rapid increase of urban areas. A key question, then, is how species cope with urbanization. It has been suggested that rural and urban conspecifics show differences in behaviour and personality. However, (i) a generalization of this phenomenon has never been made; and (ii) it is still unclear whether differences in personality traits between rural and urban conspecifics are the result of phenotypic plasticity or of intrinsic differences. In a literature review, we show that behavioural differences between rural and urban conspecifics are common and taxonomically widespread among animals, suggesting a significant ecological impact of urbanization on animal behaviour. In order to gain insight into the mechanisms leading to behavioural differences in urban individuals, we hand‐raised and kept European blackbirds (Turdus merula) from a rural and a nearby urban area under common‐garden conditions. Using these birds, we investigated individual variation in two behavioural responses to the presence of novel objects: approach to an object in a familiar area (here defined as neophilia), and avoidance of an object in a familiar foraging context (defined as neophobia). Neophilic and neophobic behaviours were mildly correlated and repeatable even across a time period of one year, indicating stable individual behavioural strategies. Blackbirds from the urban population were more neophobic and seasonally less neophilic than blackbirds from the nearby rural area. These intrinsic differences in personality traits are likely the result of microevolutionary changes, although we cannot fully exclude early developmental influences.     

Different means to the same end: long-distance migrant seabirds from two colonies differ in behaviour, despite common wintering grounds

Although seabirds that are trans-equatorial migrants show apparently broad overlap among populations in the non-breeding season, such large-scale pattern may conceal subtle but nevertheless key differences in migratory behaviour. These specializations could reflect adaptation to different environments during the breeding season, carry-over effects from the breeding to the nonbreeding period, or asymmetries in competitive ability of birds of different origin. We compared the migratory and wintering behaviour of Cory's shearwaters Calonectris diomedea nesting in Berlengas and in the Selvagens, two colonies in contrasting oceanographic environments, separated by ca. 1200 km. Although no differences were found in winter distribution, there was a marked divergence in timing, route and the use of staging areas during the postbreeding (autumn) migration. Birds from Berlengas typically travelled to oceanic waters in the North Atlantic for an extended stopover, whereas those from Selvagens rarely did so. In the South Atlantic, birds from Selvagens spent more time in flight, perhaps because they had higher energy and nutrient requirements for feather replacement compared to birds from Berlengas, which moult more flight feathers during breeding. Stable isotope analyses of feathers suggested that this variation in activity patterns was unrelated to trophic ecology. Differences in migration routes and stopovers may expose populations to distinct threats, and should be taken into consideration when defining units for conservation purposes and developing appropriate management strategies.     

Integrative tracking methods elucidate the evolutionary dynamics of a migratory divide

Migratory divides, the boundary between adjacent bird populations that migrate in different directions, are of considerable interest to evolutionary biologists because of their alleged role in speciation of migratory birds. However, the small size of many passerines has traditionally limited the tools available to track populations and as a result, restricted our ability to study how reproductive isolation might occur across a divide. Here, we integrate multiple approaches by using genetic, geolocator, and morphological data to investigate a migratory divide in hermit thrushes (Catharus guttatus). First, high genetic divergence between migratory groups indicates the divide is a region of secondary contact between historically isolated populations. Second, despite low sample sizes, geolocators reveal dramatic differences in overwintering locations and migratory distance of individuals from either side of the divide. Third, a diagnostic genetic marker that proved useful for tracking a key population suggests a likely intermediate nonbreeding location of birds from the hybrid zone. This finding, combined with lower return rates from this region, is consistent with comparatively lower fitness of hybrids, which is possibly due to this intermediate migration pattern. We discuss our results in the context of reproductive isolating mechanisms associated with migration patterns that have long been hypothesized to promote divergence across migratory divides.     

Extensive gene flow along the urban–rural gradient in a migratory colonial bird

Urban colonization by wildlife involves a combination of several different mechanisms, including phenotype or genotype sorting, phenotypic plasticity and microevolutionary adaptation. Combination of these processes can produce a rapid phenotypic, but also genetic divergence of urban versus rural populations. Here, we examined the pattern of genetic differentiation between urban and rural populations of a colonial migratory bird, the black‐headed gull Chroicocephalus ridibundus. To this end, we sampled ca 170 individuals from six (two urban and four rural) colonies in northern Poland, and genotyped them at ten microsatellite loci. Our analysis provided evidence for negligible genetic divergence of urban and rural colonies, as assessed with fixation index F_ST and Nei's unbiased genetic distance D (mean pairwise urban‐rural comparisons: F_ST = 0.003 ± 0.001 [SE] and D = 0.012 ± 0.006 [SE]). Bayesian clustering methods provided support for homogeneous genetic structure across all urban and rural populations. Also, we found no support for reduced allelic diversity in urban versus rural colonies. These results stand in a stark contrast to the previous findings on the genetic consequences of urbanization in birds. We hypothesize that this pattern could possibly be attributed to the important life‐history characters of the black‐headed gull, including coloniality, migratoriness, and high dispersal propensity. Our study provides a novel insight into the urban landscape genetics, underlining large variation in the mechanisms of urban colonization and its genetic consequences in wild animal populations.     

Seasonal niche-tracking behaviour of two partially migratory passerines

Migratory birds spend periods of the year in different locations as a response to seasonal changes in environmental suitability. They are classified as either ‘niche-trackers’ or ‘niche-switchers’, depending on whether they track or switch environmental conditions throughout the year. However, the relationship between these strategies and their migratory behaviour is still unclear. Here we examine whether migratory European Robins Erithacus rubecula and Eurasian Blackcaps Sylvia atricapilla track environmental conditions between breeding and wintering areas and whether their behaviour differs from that of their sedentary counterparts. We used ringing data for both migratory and sedentary individuals wintering sympatrically in the Iberian Peninsula to assess the environmental conditions relating to their seasonal distributions. We explored seasonal niche-tracking using two multivariate analyses with alternative sets of predictor variables (landscape and climate) to generate different environmental scenarios. Our results show that migratory individuals track similar climatic conditions throughout their seasonal distributions, whereas sedentary birds cope with great variation in climate over the course of the year. In addition, migratory birds show less seasonal overlap in the landscape structure of their chosen habitats compared with sedentary individuals. These results suggest that there is a trade-off between, on the one hand, the cost for migrants of travelling long distances and, on the other, the increased flexibility required by sedentary birds if they are to tolerate a wider suite of environmental conditions within their permanent ranges. Given that sedentary populations in the southern Iberian Peninsula seem to be linked to populations of migratory individuals of these two species that started to move northwards after the last glacial cycle, the observed patterns suggest that migrant birds represent a fraction of the southern population that is specialized in the exploitation of a narrower range of environmental conditions.     

Urban behavioural adaptation

A large and growing proportion of the world is impacted directly by human activities; among the most extreme of these is the spread of urban environments. Environmental change associated with urbanization represents a potentially potent source of selection. While urban environments generally have lowered biodiversity, some clades seem to thrive in urban settings. For example, many members of the bird family Turdidae, known as the ‘true thrushes’ and the blackbird Turdus merula (Fig. 1) in particular, are familiar urban species. Indeed, the colonization of urban environments by blackbirds has become a textbook case study for our understanding of the many ways a wild species can deal with urbanization. In this issue, Mueller et al. (Molecular Ecology, 00, 2013, 00) add to that story by beginning to address the genetic nature of behavioural adaptation of blackbirds colonizing urban areas. They do this by testing for divergence between paired urban and rural samples at a suite of candidate genes with hypothesized effects on behaviours thought to be important for the colonization of urban environments. They find evidence for consistent patterns of divergence at an exonic microsatellite associated with the SERT gene. SERT has a number of hypothesized behavioural effects, including harm avoidance, which may be associated with tolerating the hustle and bustle of urban environments. This is among the first evidence that behavioural differences between urban and rural environments have a genetic basis and this work suggests that urban environments can in some cases exert homogeneous selection pressures.     

Postglacial northward expansion and genetic differentiation between migratory and sedentary populations of the broad‐tailed hummingbird (Selasphorus platycercus)

Unlike other migratory hummingbirds in North America, the broad‐tailed hummingbird (Selasphorus platycercus) exhibits both long‐distance migratory behaviour in the USA and sedentary behaviour in Mexico and Guatemala. We examined the evolution of migration linked to its northward expansion using a multiperspective approach. We analysed variation in morphology, mitochondrial and nuclear DNA, estimated migration rates between migratory and sedentary populations, compared divergence times with the occurrence of Quaternary climate events and constructed species distribution models to predict where migratory and sedentary populations resided during the Last Glacial Maximum (LGM) and Last Interglacial (LIG) events. Our results are consistent with a recent northward population expansion driven by migration from southern sedentary populations. Phylogeographical analyses and population genetics methods revealed that migratory populations in the USA and sedentary populations in Mexico of the platycercus subspecies form one admixed population, and that sedentary populations from southern Mexico and Guatemala (guatemalae) undertook independent evolutionary trajectories. Species distribution modelling revealed that the species is a niche tracker and that the climate conditions associated with modern obligate migrants in the USA were not present during the LIG, which provides indirect evidence for recent migratory behaviour in broad‐tailed hummingbirds on the temporal scale of glacial cycles. The finding that platycercus hummingbirds form one genetic population and that suitable habitat for migratory populations was observed in eastern Mexico during the LIG also suggests that the conservation of overwintering sites is crucial for obligate migratory populations currently facing climate change effects.     

Acoustic but no genetic divergence in migratory and sedentary populations of blackcaps,Sylvia atricapilla

In songbirds, territorial songs are key regulators of sexual selection and are learned from conspecifics. The cultural transmission of songs leads to divergence in song characteristics within populations, which can ultimately lead to speciation. Many songbirds also migrate, and individual differences in migratory behaviours can influence population genetic structure and local song differentiation. Blackcaps, Sylvia atricapilla, exhibit versatile territorial songs and show diversity in migration behaviours. They therefore comprise a good model for investigating the relationships between migratory patterns, song variation, and genetic diversity. We studied a migratory population (two groups near Paris) and a sedentary population (three groups in Corsica). All of the birds were ringed and blood sampled to investigate genetic relatedness using 17 microsatellite loci. A detailed song analysis showed that this species has a complex repertoire (> 100 syllables), which required the development of a semi‐supervised method to classify different categories of syllables and compare sequences of syllables. Our analysis showed no genetic structuring among populations: individuals belonging to the same group were not genetically closer than those from different groups. However, we found a strong wingsize difference between sedentary and migratory populations. We also showed that geographical variations in songs rely at least on both syllable and sequence content. Unexpectedly, despite a higher turnover of individuals, migratory groups share as many syllables and sequences as sedentary groups, which raises interesting issues on song learning and the maintenance of dialects in migratory birds.     

Does light pollution alter daylength? A test using light loggers on free-ranging European blackbirds (Turdus merula)

Artificial light at night is one of the most apparent environmental changes accompanying anthropogenic habitat change. The global increase in light pollution poses new challenges to wild species, but we still have limited understanding of the temporal and spatial pattern of exposure to light at night. In particular, it has been suggested by several studies that animals exposed to light pollution, such as songbirds, perceive a longer daylength compared with conspecifics living in natural darker areas, but direct tests of such a hypothesis are still lacking. Here, we use a combination of light loggers deployed on individual European blackbirds, as well as automated radio-telemetry, to examine whether urban birds are exposed to a longer daylength than forest counterparts. We first used activity data from forest birds to determine the level of light intensity which defines the onset and offset of daily activity in rural areas. We then used this value as threshold to calculate the subjective perceived daylength of both forest and urban blackbirds. In March, when reproductive growth occurs, urban birds were exposed on average to a 49-min longer subjective perceived daylength than forest ones, which corresponds to a 19-day difference in photoperiod at this time of the year. In the field, urban blackbirds reached reproductive maturity 19 day earlier than rural birds, suggesting that light pollution could be responsible of most of the variation in reproductive timing found between urban and rural dwellers. We conclude that light at night is the most relevant change in ambient light affecting biological rhythms in avian urban-dwellers, most likely via a modification of the perceived photoperiod.     

Loss of migration and urbanization in birds: a case study of the blackbird (Turdus merula)

Many organisms have invaded urban habitats, although the underlying factors initially promoting urbanization remain poorly understood. Partial migration may facilitate urbanization because such populations benefit from surplus food in urban environments during winter, and hence enjoy reduced fitness costs of migratory deaths. We tested this hypothesis in the European blackbird Turdus merula, which has been urbanized since the 19th century, by compiling information on timing of urbanization, migratory status, and population density for 99 cities across the continent. Timing of urbanization was spatially auto-correlated at scales up to 600 km. Analyses of timing of urbanization revealed that urbanization occurred earlier in partially migratory and resident populations than in migratory populations of blackbirds. Independently, this effect was most pronounced in the range of the distribution that currently has the highest population density, suggesting that urbanization facilitated population growth. These findings are consistent with the hypothesis that timing of urbanization is facilitated by partial migration, resulting in subsequent residency and population growth.     

Do xeric landscapes increase genetic divergence in aquatic ecosystems?

1. Previous investigations of the ecological genetics among amphipods in south-western U.S.A. suggested a xeric landscape promoted genetic divergence among passively dispersed freshwater invertebrates, thereby enhancing speciation events. We predicted that less divergence would occur among amphipod populations across similar geographic distances in mesic regions. 2. Eight Hyalella azteca populations were sampled along a 200-km transect in western Oregon, U.S.A. Genetic distances among populations were estimated from randomly amplified polymorphic DNA (RAPD). Genetic analyses indicated much less divergence among Oregon populations than among Arizona populations in an arid environment. 3. Behavioural observations support the genetic data: Oregon populations exhibit little differentiation in swimming behaviour, whereas Hyalella populations in Arizona exhibit extremes in swimming behaviour. 4. These results provide preliminary support for the hypothesis that a xeric landscape promotes genetic and behavioural divergence among amphipods. Many aquatic invertebrates classified as panmictic populations may encompass genetically distinct groups; those isolated by a xeric landscape are especially prone to diversification.     

Phylogeography of the Ryukyu robin (Erithacus komadori): population subdivision in land-bridge islands in relation to the shift in migratory habit

We analysed the mitochondrial control region sequences of 150 Ryukyu robins (Erithacus komadori) from five migratory and three sedentary populations. E. komadori is endemic to the subtropical Asian islands, is well differentiated among populations in morphology and migratory behaviour within its narrow habitat range, and is ideal for examining the effects of altered migratory habits on population differentiation. Maximum-likelihood analysis among the haplotypes resulted in the generation of a single tree in which two phylogenetic clades corresponding to the two subspecies were evident. Within the northern lineage, three distinctive subgroups of populations (one migratory and two sedentary groups) were observed by population genetic analysis. The migration-related wing morphology and molecular data were then compared among groups. The wing shape of the northern lineage was significantly more pointed than that of the southern sedentary lineage, and they were exclusively discriminated from each other. The difference was not so apparent between the sedentary and migratory groups within the northern lineage, suggesting that the present northern subspecies is primarily a migratory lineage. The different migratory behaviours of the robin played an apparent role in maintaining the genetic structure at two different levels--one between the southern and northern lineages and the other between the sedentary and migratory groups within the northern lineage. While gene flow had long been maintained among the islands occupied by migratory individuals, migrants have been unable to contribute to the gene pool of the sedentary populations despite passing through the breeding range of such populations twice each year.     

The genetic structure of the European breeding populations of a declining farmland bird,the ortolan bunting (<Emphasis Type="Italic">Emberiza hortulana</Emphasis>), reveals conservation priorities

Anthropogenic activities, such as agricultural intensification, caused large declines in biodiversity, including farmland birds. In addition to demographic consequences, anthropogenic activities can result in loss of genetic diversity, reduction of gene flow and altered genetic structure. We investigated the distribution of the genetic variation of a declining farmland and long-distance migratory bird, the ortolan bunting Emberiza hortulana, across its European breeding range to assess the impact of human-driven population declines on genetic diversity and structure in order to advise conservation priorities. The large population declines observed have not resulted in dramatic loss of genetic diversity, which is moderate to high and constant across all sampled breeding sites. Extensive gene flow occurs across the breeding range, even across a migratory divide, which contributes little to genetic structuring. However, gene flow is asymmetric, with the large eastern populations acting as source populations for the smaller western ones. Furthermore, breeding populations that underwent the largest declines, in Fennoscandia and Baltic countries, appear to be recently isolated, with no gene exchange occurring with the eastern or the western populations. These are signs for concern as declines in the eastern populations could affect the strength of gene flow and in turn affect the western populations. The genetic, and demographic, isolation of the northern populations make them particularly sensitive to loss of genetic diversity and to extinction as no immigration is occurring to counter-act the drastic declines. In such a situation, conservation efforts are needed across the whole breeding range: in particular, protecting the eastern populations due to their key role in maintaining gene flow across the range, and focussing on the northern populations due to their recent isolation and endangered status.