Bergmann's rule in alien birds

Native bird species show latitudinal gradients in body size across species (Bergmann's rule), but whether or not such gradients are recapitulated in the alien distributions of bird species are unknown. Here, we test for the existence of Bergmann's rule in alien bird species worldwide, and investigate the causes of the observed patterns. Published databases were used to obtain the worldwide distributions of established alien bird populations, the locations of alien bird introductions, and bird body masses. Randomisation tests and linear models were used to assess latitudinal patterns in the body masses of introduced and established alien bird populations. Established alien bird species exhibit Bergmann's rule, but this is largely explained by where alien bird species have been introduced: latitudinal variation in the body masses of established alien bird species simply reflects latitudinal variation in the body masses of introduced species. There is some evidence that body mass is implicated in whether or not established species’ alien ranges spread towards or contract away from the Equator following establishment. However, most alien bird ranges are encompassed by the latitudinal band(s) to which the species was introduced. Bergmann's rule in alien birds is therefore a consequence of where humans have introduced different species, rather than of natural processes operating after population introduction.     

Colonisation of urban environments is associated with reduced migratory behaviour,facilitating divergence from ancestral populations

How individuals colonising novel environments overcome the diverse suite of new selection pressures is a fundamental question in ecology and evolution. Urban environments differ markedly from the rural ones that they replace and successful colonisation of urban areas may therefore require local adaptation and phenotypic/genetic divergence from ancestral populations. Such a process would be facilitated by limited dispersal to and from the novel habitat. Here we assess divergence in migratory behaviour between seven pairs of urban and rural European blackbird Turdus merula populations along a 2800 km transect across Europe. This former forest specialist is now amongst the most abundant urban birds across most of its range. We use a stable isotope approach due to the lack of sufficient ringing data from multiple urban populations, and compare hydrogen isotopic ratios of tissues grown in the breeding (feathers) and wintering areas (claws) to derive an index of long distance migratory behaviour. We find a tendency for urban blackbirds to be more sedentary than rural ones at all sites and this divergence is particularly strong at the north‐eastern limit of our transect, i.e. in Estonia and Latvia. These urban populations are those that have been established most recently (from the late 1930s to 1950s) implying that urbanisation can promote rapid ecological divergence. The increased sedentary behaviour of urban birds could promote further ecological divergence between rural and urban populations, such as the earlier breeding of urban blackbirds, and in some cases may contribute to their previously documented 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.     

Urbanization disrupts latitude‐size rule in 17‐year cicadas

Many ectotherms show a decrease in body size with increasing latitude due to changes in climate, a pattern termed converse Bergmann's rule. Urban conditions—particularly warmer temperatures and fragmented landscapes—may impose stresses on development that could disrupt these body size patterns. To test the impact of urbanization on development and latitudinal trends in body size, we launched a citizen science project to collect periodical cicadas (Magicicada septendecim) from across their latitudinal range during the 2013 emergence of Brood II. Periodical cicadas are long‐lived insects whose distribution spans a broad latitudinal range covering both urban and rural habitats. We used a geometric morphometric approach to assess body size and developmental stress based on fluctuating asymmetry in wing shape. Body size of rural cicadas followed converse Bergmann's rule, but this pattern was disrupted in urban habitats. In the north, urban cicadas were larger than their rural counterparts, while southern populations showed little variation in body size between habitats. We detected no evidence of differences in developmental stress due to urbanization. To our knowledge, this is the first evidence that urbanization disrupts biogeographical trends in body size, and this pattern highlights how the effects of urbanization may differ over a species’ range.     

Patterns of contact call differentiation in the panmictic East African Abyssinian White‐eye Zosterops abyssinicus (Aves: Passeriformes)

Species distribution patterns range from highly disjunct to continuous, depending on their ecological demands and the availability of respective habitats. East African savannahs are mostly interconnected and ecologically comparatively homogenous and thus provide a prerequisite for a rather panmictic distribution pattern for species occurring in this habitat. The Abyssinian white‐eye Zosterops abyssinicus is a savannah inhabiting bird species, representing such a continuous distribution. This species occurs in high abundances and is very mobile, and past population genetic studies have suggested that gene flow is high and genetic differentiation is low even across relatively large geographic distances. Further, only little morphological differences were found. In order to test for potential divergence in acoustic traits despite its interconnected geographic distribution, we analyzed 2795 contact calls of Z. abyssinicus, which were recorded at 19 sites across Kenya. Our data indicate weak, but significant differentiation in call characteristics across latitudinal gradients. We found strong changes in call characteristics in populations where Z. abyssinicus occurs in sympatry with its highland congener, Zosterops poliogaster. However, the changes in call characteristics in sympatry were in different directions and lead to strong differentiation of the sympatric populations to other conspecific populations potentially representing a case of cascade reinforcement. The detected spatial gradients likely result from ecological differences and balancing effects of natural and sexual selection.     

High urban population density of birds reflects their timing of urbanization

Living organisms generally occur at the highest population density in the most suitable habitat. Therefore, invasion of and adaptation to novel habitats imply a gradual increase in population density, from that at or below what was found in the ancestral habitat to a density that may reach higher levels in the novel habitat following adaptation to that habitat. We tested this prediction of invasion biology by analyzing data on population density of breeding birds in their ancestral rural habitats and in matched nearby urban habitats that have been colonized recently across a continental latitudinal gradient. We estimated population density in the two types of habitats using extensive point census bird counts, and we obtained information on the year of urbanization when population density in urban habitats reached levels higher than that of the ancestral rural habitat from published records and estimates by experienced ornithologists. Both the difference in population density between urban and rural habitats and the year of urbanization were significantly repeatable when analyzing multiple populations of the same species across Europe. Population density was on average 30 % higher in urban than in rural habitats, although density reached as much as 100-fold higher in urban habitats in some species. Invasive urban bird species that colonized urban environments over a long period achieved the largest increases in population density compared to their ancestral rural habitats. This was independent of whether species were anciently or recently urbanized, providing a unique cross-validation of timing of urban invasions. These results suggest that successful invasion of urban habitats was associated with gradual adaptation to these habitats as shown by a significant increase in population density in urban habitats over time.     

A conceptual framework for the colonisation of urban areas: the blackbird Turdus merula as a case study

Despite increasing interest in urban ecology the factors limiting the colonisation of towns and cities by species from rural areas are poorly understood. This is largely due to the lack of a detailed conceptual framework for this urbanisation process, and of sufficient case studies. Here, we develop such a framework. This draws upon a wide range of ecological and evolutionary theory and the increasing number of studies of how the markedly divergent conditions in urban and rural areas influence the traits of urban populations and the structure of urban assemblages. We illustrate the importance of this framework by compiling a detailed case study of spatial and temporal variation in the urbanisation of the blackbird Turdus merula. Our framework identifies three separate stages in the urbanisation process: (i) arrival, (ii) adjustment, and (iii) spread. The rate of progress through each stage is influenced by environmental factors, especially human attitudes and socio‐economic factors that determine the history of urban development and the quality of urban habitats, and by species' ecological and life‐history traits. Some traits can positively influence progression through one stage, but delay progression through another. Rigorous assessment of the factors influencing urbanisation should thus ideally pay attention to the different stages. Urbanisation has some similarities to invasion of exotic species, but the two clearly differ. Invasion concerns geographic range expansion that is external to the species' original geographic range, whilst urbanisation typically relates to filling gaps within a species' original range. This process is exemplified by the blackbird which is now one of the commonest urban bird species throughout its Western Palearctic range. This is in stark contrast to the situation 150 years ago when the species was principally confined to forest. Blackbird urbanisation was first recorded in Germany in 1820, yet some European cities still lack urban blackbirds. This is especially so in the east, where urbanisation has spread more slowly than in the west. The timing of blackbird urbanisation exhibits a marked spatial pattern, with latitude and longitude explaining 76% of the variation. This strong spatial pattern contrasts with the weaker spatial pattern in timing of urbanisation exhibited by the woodpigeon Columba palumbus (with location explaining 39% of the variation), and with the very weak spatial pattern in timing of black‐billed magpie Pica pica urbanisation (in which location explains 12% of the variation). Strong spatial patterns in timing of urbanisation are more compatible with the leap‐frog urbanisation model, in which urban adapted or imprinted birds colonise other towns and cities, than with the independent urbanisation model, in which urban colonisation events occur independently of each other. Spatial patterns in isolation do not, however, confirm one particular model. Factors relating to the arrival and adjustment stages appear particularly likely to have influenced the timing of blackbird urbanisation. Spatial variation in the occurrence of urban populations and the timing of their establishment creates opportunities to assess the factors regulating urbanisation rates, and how the composition of urban assemblages develops as a result. These are major issues for urban ecology.     

Is urbanisation of European blackbirds (Turdus merula) associated with genetic differentiation?

Because of the extreme ecological and environmental changes along an urban–rural gradient, it has been proposed that urbanised and non-urbanised populations of the same species may be distinctly isolated. There is evidence that urban populations have become significantly different from the original forest populations in several aspects. However, little is known about the extent to which urban and non-urban populations are genetically isolated from each other. We tested the hypothesis of genetic differentiation by comparing the genomic DNA of an urban and a nearby forest-living European blackbird (Turdus merula) population. The present results suggest that, based on amplified fragment length polymorphism analysis, the urban population studied is very similar to a forest population at neutral genetic markers. Thus, despite indications of obvious functional genetic adaptation, the hypothesis of an overall genetic differentiation between our urban and forest populations could not be supported.Eberhard Gwinner died on 7 September 2004     

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.     

Divergence with gene flow and fine-scale phylogeographical structure in the wedge-billed woodcreeper, Glyphorynchus spirurus, a Neotropical rainforest bird

Determining the relative roles of vicariance and selection in restricting gene flow between populations is of central importance to the evolutionary process of population divergence and speciation. Here we use molecular and morphological data to contrast the effect of isolation (by mountains and geographical distance) with that of ecological factors (altitudinal gradients) in promoting differentiation in the wedge-billed woodcreeper, Glyphorynchus spirurus , a tropical forest bird, in Ecuador. Tarsus length and beak size increased relative to body size with altitude on both sides of the Andes, and were correlated with the amount of moss on tree trunks, suggesting the role of selection in driving adaptive divergence. In contrast, molecular data revealed a considerable degree of admixture along these altitudinal gradients, suggesting that adaptive divergence in morphological traits has occurred in the presence of gene flow. As suggested by mitochondrial DNA sequence data, the Andes act as a barrier to gene flow between ancient subspecific lineages. Genome-wide amplified fragment length polymorphism markers reflected more recent patterns of gene flow and revealed fine-scale patterns of population differentiation that were not detectable with mitochondrial DNA, including the differentiation of isolated coastal populations west of the Andes. Our results support the predominant role of geographical isolation in driving genetic differentiation in G. spirurus , yet suggest the role of selection in driving parallel morphological divergence along ecological gradients.     

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.     

Reproductive interactions of the Shiny Cowbird Molothrus bonariensis and the Yellow-hooded Blackbird Agelaius icterocephalus in Trinidad

The reproductive interactions of the Shiny Cowbird Molothrus bonariensis , a brood parasite, and the Yellow-hooded Blackbird Agelaius icterocephalus , a host of the cowbird, were studied In Trinidad, West Indies. We gathered information on the breeding biology of the Shiny Cowbird and the Yellow-hooded Blackbird, the frequency of use of the host species, and the effects of brood parasitism on host breeding success. Yellow-hooded Blackbirds are polygynous for the most part; males build nests and attempt to attract females to lay in them by means of song and visual displays directed towards the nests. This behaviour probably makes it easy for cowbirds to locate breeding birds and their nests. Cowbird eggs were found in 153 of 377 (40–3 %) blackbird nests located before the nestling stage. Shiny Cowbird parasitism of the Yellow-hooded Blackbird had little negative impact on host reproductive success, whereas predation accounted for the majority of nest failures. Vigilant nest defense by male blackbirds combined with colonial breeding apparently also minimized the extent of host egg damage and removal by cowbirds, and the parasitized and unparasitized nests were equally successful at producing blackbirds. Cowbirds most frequently parasitized the first or only nesting attempts in blackbird territories, and first or only nests were also successful more frequently than subsequent nests.     

Thrushes now largely restricted to the built environment in eastern England

Abstract.  I studied the distribution and density of three thrush populations, blackbird Turdus merula , song thrush T. philomelos and mistle thrush T. viscivorus , in an urban and contiguous rural area, totalling 2636 ha, in eastern England. Populations of these species are declining and I found 826, 85 and 30 territories of blackbird, song thrush and mistle thrush, respectively. Significantly more territories of all species than expected were within the urban boundary. Significantly more territories than expected were found of all three species in the built environment (residential housing, factories, schools, etc. with their associated gardens and green-space), urban and rural areas combined. Farmland occupied 67% of the study area but held significantly fewer blackbird and mistle thrush territories than expected, associated mainly with the small amount of grass; song thrushes were not recorded on farmland. Rural woodland and scrub held more blackbird and song thrush territories than expected. Song thrush was significantly associated with scrub within the urban boundary. With all three species largely absent from farmland, residential habitats can be considered as habitat refuges. The consequences of this for conservation and planning are discussed.     

Low genetic and morphological differentiation between an introduced population of dunnocks in New Zealand and an ancestral population in England

Species invasions and exotic species introductions can be considered as ??unplanned experiments??, which help us to understand the evolution of organisms. In this study, we investigated whether an exotic bird species, the dunnock (Prunella modularis), has diverged genetically and morphologically from its native source population (Cambridge, England) after introduction into a new environment (Dunedin, South Island of New Zealand; exotic population). We used a set of microsatellite markers and three morphological traits to quantify the divergence between these two populations. We quantified neutral genotypic differentiation between the populations, and also used an individual-based Bayesian clustering method to assess genetic structure. We compared morphological divergence using univariate and principal components analyses. We found that individuals from the Dunedin population are genetically distinct from the Cambridge population, but levels of differentiation are very low. Overall within-population levels of genetic diversity are low compared to other bird species, and effective population sizes are small; indicating that the native population probably has a historically low level of genetic diversity, and that the introduced population retained most of that diversity after its introduction into New Zealand. We found little evidence of morphological divergence, and the evolutionary rate of change in these traits is below the average for other taxa. Our study adds support to the growing literature showing that invasive species maintain most of their initial genetic diversity after multiple founder events, even when population size is severely reduced. Moreover, our morphological data indicate slow evolutionary rates in species introduced to similar habitats.     

Genomic signatures of rapid adaptive divergence in a tropical montane species

Mountain regions contain extraordinary biodiversity. The environmental heterogeneity and glacial cycles often accelerate speciation and adaptation of montane species, but how these processes influence the genomic differentiation of these species is largely unknown. Using a novel chromosome-level genome and population genomic comparisons, we study allopatric divergence and selection in an iconic bird living in a tropical mountain region in New Guinea, Archbold''s bowerbird (Amblyornis papuensis). Our results show that the two populations inhabiting the eastern and western Central Range became isolated ca 11 800 years ago, probably because the suitable habitats for this cold-tolerating bird decreased when the climate got warmer. Our genomic scans detect that genes in highly divergent genomic regions are over-represented in developmental processes, which is probably associated with the observed differences in body size between the populations. Overall, our results suggest that environmental differences between the eastern and western Central Range probably drive adaptive divergence between them.     

Laying‐sequence variation in yolk carotenoids and egg characteristics in the red‐winged blackbird Agelaius phoeniceus

In many bird species with asynchronous hatching, smaller, later‐hatched nestlings are out‐competed for food by their larger, earlier‐hatched siblings and therefore suffer increased mortality via starvation. It is thought that female birds can either maintain or reduce the survival disadvantage of later‐hatched nestlings by differentially allocating maternal resources across the eggs of a clutch. Carotenoid pigments are an example of resources that female birds allocate differentially when producing a clutch, but laying sequence patterns for these pigments remain poorly studied in North American songbirds. We examined intraclutch variation in yolk carotenoids and egg metrics in 27 full clutches of red‐winged blackbird Agelaius phoeniceus eggs collected from eight wetlands in central Alberta, Canada. We predicted that carotenoids would decrease across the laying sequence, as in this species, later‐hatched, marginal nestlings suffer greater mortality than earlier‐hatched, core nestlings. We found nine carotenoid pigments in red‐winged blackbird egg yolks, including two that have never been described from avian yolks: α‐doradexanthin and adonirubin. As predicted, concentrations and amounts of most carotenoids decreased across the laying sequence, suggesting that female red‐winged blackbirds depleted their carotenoid resources as they laid more eggs. However, egg mass and yolk mass both increased across the laying sequence, suggesting that female red‐winged blackbirds may use other maternal resources to compensate for the size and survival disadvantage experienced by later‐hatched, marginal nestlings.     

Genetic and morphological divergence between Littorina fabalis ecotypes in Northern Europe

Low dispersal marine intertidal species facing strong divergent selective pressures associated with steep environmental gradients have a great potential to inform us about local adaptation and reproductive isolation. Among these, gastropods of the genus Littorina offer a unique system to study parallel phenotypic divergence resulting from adaptation to different habitats related with wave exposure. In this study, we focused on two Littorina fabalis ecotypes from Northern European shores and compared patterns of habitat‐related phenotypic and genetic divergence across three different geographic levels (local, regional and global). Geometric morphometric analyses revealed that individuals from habitats moderately exposed to waves usually present a larger shell size with a wider aperture than those from sheltered habitats. The phenotypic clustering of L. fabalis by habitat across most locations (mainly in terms of shell size) support an important role of ecology in morphological divergence. A genome scan based on amplified fragment length polymorphisms (AFLPs) revealed a heterogeneous pattern of differentiation across the genome between populations from the two different habitats, suggesting ecotype divergence in the presence of gene flow. The contrasting patterns of genetic structure between nonoutlier and outlier loci, and the decreased sharing of outlier loci with geographic distance among locations are compatible with parallel evolution of phenotypic divergence, with an important contribution of gene flow and/or ancestral variation. In the future, model‐based inference studies based on sequence data across the entire genome will help unravelling these evolutionary hypotheses, improving our knowledge about adaptation and its influence on diversification within the marine realm.     

Shifting latitudinal clines in avian body size correlate with global warming in Australian passerines

Intraspecific latitudinal clines in the body size of terrestrial vertebrates, where members of the same species are larger at higher latitudes, are widely interpreted as evidence for natural selection and adaptation to local climate. These clines are predicted to shift in response to climate change. We used museum specimens to measure changes in the body size of eight passerine bird species from south-eastern Australia over approximately the last 100 years. Four species showed significant decreases in body size (1.8–3.6% of wing length) and a shift in latitudinal cline over that period, and a meta-analysis demonstrated a consistent trend across all eight species. Southern high-latitude populations now display the body sizes typical of more northern populations pre-1950, equivalent to a 7° shift in latitude. Using ptilochronology, we found no evidence that these morphological changes were a plastic response to changes in nutrition, a likely non-genetic mechanism for the pattern observed. Our results demonstrate a generalized response by eight avian species to some major environmental change over the last 100 years or so, probably global warming.     

Effects of urbanisation on disease prevalence and age structure in blackbird Turdus merula populations

Despite increasing interest in urban ecology most attention has focussed on describing changes in assemblage composition and structure along urbanisation gradients, whilst relatively little research has focussed on the mechanisms behind these changes. Ecological theory predicts that alterations in biotic interactions are particularly likely to arise, especially with regard to disease risk. Here, we report on differences in prevalence of avian malaria and tick infection and intensity in 11 paired urban and rural blackbird Turdus merula populations from across the western Palearctic. We find large and consistent reductions in tick prevalence and intensity in urban areas. There are also large reductions in the prevalence of avian malaria in many, but not all, urban areas. The proportion of first year birds in urban populations is significantly lower than that in rural ones, and across the more natural rural sites southerly populations contain fewer first years than northern ones. These patterns are expected to arise if survival rates are higher in urban areas, and are negatively correlated with latitude.     

Intra- and interspecific morphological variation in the field mouse species Apodemus argenteus and A. speciosus in the Japanese archipelago: the role of insular isolation and biogeographic gradients

Two species of field mice, Apodemus argenteus and A. speciosus, occur in sympatry across the Japanese archipelago. The inter- and intraspecific patterns of morphological differentiation have been evaluated, using a Fourier analysis of the mandible outline. The relative importance of the effect of insular isolation and latitudinal climatic gradient on the size and shape of the two species was assessed by a comparison of the populations from the large island of Honshu and the surrounding small-island populations. The size variation in A. argenteus is correlated with the climatic gradient whilst the shape variation corresponds mainly to a random differentiation of the small-island populations from a Honshu-like basic morphological pattern. A. speciosus displays increased size on small islands, and its shape variation is related to both the climatic gradient and insularity. Finally, the two species are differentiated by both the size and shape of the mandible across the Japanese archipelago, suggesting that interspecific competition between both species is reduced via niche partitioning. Our results emphasize the importance of insular isolation on shape differentiation, but a part of the morphological differentiation is also related to the latitudinal climatic gradient. Isolation on small islands could have favoured such a response to environmental factors by lowering the gene flow that prevents almost any significant differentiation within Honshu populations.