Candidate gene polymorphisms for behavioural adaptations during urbanization in blackbirds

Mueller, Jakob C.; Partecke, Jesko; Hatchwell, Ben J.; Gaston, Kevin J.; Evans, Karl L.

doi:10.1111/mec.12288

Cited by 138 publications

(150 citation statements)

References 55 publications

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“…These findings are matched by observations in this study and in the parallel study of effects of food availability on other nests at our sites (Pollock et al, 2017). In addition to immediate effects of the environment on developing offspring, such differences could also reflect prenatal maternal investment (e.g., differences in egg composition, Toledo et al, 2016) or genetic differences between urban and rural populations (Mueller et al, 2013). Our cross-fostering experiment does not support these latter hypotheses as we found no strong effects of natal origin on reproductive and fitness traits (Figure 3).…”

Section: Discussionsupporting

confidence: 72%

Elevated Immune Gene Expression Is Associated with Poor Reproductive Success of Urban Blue Tits

et al. 2017

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Urban and forest habitats differ in many aspects that can lead to modifications of the immune system of wild animals. Altered parasite communities, pollution, and artificial light at night in cities have been associated with exacerbated inflammatory responses, with possibly negative fitness consequences, but few data are available from free-living animals. Here, we investigate how urbanization affects major immune pathways and experimentally test potentially contributing factors in blue tits (Cyanistes caeruleus) from an urban and forest site. We first compared breeding adults by quantifying the mRNA transcript levels of proteins associated with anti-bacterial, anti-malarial (TLR4, LY86) and anti-helminthic (Type 2 transcription factor GATA3) immune responses. Adult urban and forest blue tits differed in gene expression, with significantly increased TLR4 and GATA3, but not LY86, in the city. We then experimentally tested whether these differences were environmentally induced by cross-fostering eggs between the sites and measuring mRNA transcripts in nestlings. The populations differed in reduced reproductive success, with a lower fledging success and lower fledgling weight recorded at the urban site. This mirrors the findings of our twin study reporting that the urban site was severely resource limited when compared to the forest. Because of low urban survival, robust gene expression data were only obtained from nestlings reared in the forest. Transcript levels in these nestlings showed no (TLR4, LY86), or weak (GATA3), differences according to their origin from forest or city nests, suggesting little genetic or maternal contribution to nestling immune transcript levels. Lastly, to investigate differences in parasite pressure between urban and forest sites, we measured the prevalence of malaria in adult and nestling blood. Prevalence was invariably high across environments and not associated with the transcript levels of the studied immune genes. Our results support the hypothesis that inflammatory pathways are activated in an urban environment and suggest that these differences are most likely induced by environmental factors.

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Section: Discussionsupporting

confidence: 72%

Elevated Immune Gene Expression Is Associated with Poor Reproductive Success of Urban Blue Tits

et al. 2017

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“…11,12,43 More recently, the SERT gene has been suggested as one of the candidate genes for local adaptation to novel conditions and urbanization. 13 Since we found that one of the main differences between urban and forest great tits probably relied on personality, 27,44 we thought that it could be valuable to look for a direct relationship between SERT polymorphisms, in addition to DRD4, and personality. Out of 21 SNPs (10 SNPs in DRD4 and 11 SNPs in SERT), we found a highly significant association Figure 4.…”

Section: Discussionmentioning

confidence: 99%

“…The urban habitat, due to rapid changes in diet as well as environmental pollution, is undoubtedly impacting not only the human epigenome, but also the evolution of many other species. Since urban habitats have independently been found to affect levels of DNA methylation through pollution effects 25 and also personality traits, 13 we hypothesize that differences in personality between urban and forest Parus major populations could be related to variation in methylation.…”

Section: Introductionmentioning

confidence: 99%

“…A recent study on 12 paired urban and rural populations of the blackbird Turdus merula found a highly significant divergence at an exonic microsatellite of SERT gene between habitats. 13 They concluded that the SERT gene can be considered as one of the candidate loci for local adaptation to novel conditions and urbanization. Hence, the possible gene-environment interaction has been suggested in both DRD4 and SERT genes.…”

Section: Introductionmentioning

confidence: 99%

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Combined epigenetic and intraspecific variation of theDRD4andSERTgenes influence novelty seeking behavior in great titParus major

et al. 2015

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DNA methylation is one of the main epigenetic mechanisms that can regulate gene expression and is an important means for creating phenotypic variation. In the present study, we performed methylation profiling of 2 candidate genes for personality traits, namely DRD4 and SERT, in the great tit Parus major to ascertain whether personality traits and behavior within different habitats have evolved with the aid of epigenetic variation. We applied bisulphite PCR and strand-specific sequencing to determine the methylation profile of the CpG dinucleotides in the DRD4 and SERT promoters and also in the CpG island overlapping DRD4 exon 3. Furthermore, we performed pyrosequencing to quantify the total methylation levels at each CpG location. Our results indicated that methylation was »1-4% higher in urban than in forest birds, for all loci and tissues analyzed, suggesting that this epigenetic modification is influenced by environmental conditions. Screening of genomic DNA sequence revealed that the SERT promoter is CpG poor region. The methylation at a single CpG dinucleotide located 288 bp from the transcription start site was related to exploration score in urban birds. In addition, the genotypes of the SERT polymorphism SNP234 located within the minimal promoter were significantly correlated with novelty seeking behavior in captivity, with the allele increasing this behavior being more frequent in urban birds. As a conclusion, it seems that both genetic and methylation variability of the SERT gene have an important role in shaping personality traits in great tits, whereas genetic and methylation variation at the DRD4 gene is not strongly involved in behavior and personality traits.

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“…selection [11,12]. For example, a study of Peromyscus leucopus mice transcriptomes in New York City (NYC) identified several plausible adaptive changes associated with urbanization, but did not quantify phenotypic changes in the mice.…”

Section: Introductionmentioning

confidence: 99%

Urbanization drives the evolution of parallel clines in plant populations

2016

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Urban ecosystems are an increasingly dominant feature of terrestrial landscapes. While evidence that species can adapt to urban environments is accumulating, the mechanisms through which urbanization imposes natural selection on populations are poorly understood. The identification of adaptive phenotypic changes (i.e. clines) along urbanization gradients would facilitate our understanding of the selective factors driving adaptation in cities. Here, we test for phenotypic clines in urban ecosystems by sampling the frequency of a Mendelian-inherited trait-cyanogenesis-in white clover (Trifolium repens L.) populations along urbanization gradients in four cities. Cyanogenesis protects plants from herbivores, but reduces tolerance to freezing temperatures. We found that the frequency of cyanogenic plants within populations decreased towards the urban centre in three of four cities. A field experiment indicated that spatial variation in herbivory is unlikely to explain these clines. Rather, colder minimum winter ground temperatures in urban areas compared with non-urban areas, caused by reduced snow cover in cities, may select against cyanogenesis. In the city with no cline, high snow cover might protect plants from freezing damage in the city centre. Our study suggests that populations are adapting to urbanization gradients, but regional climatic patterns may ultimately determine whether adaptation occurs.

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Candidate gene polymorphisms for behavioural adaptations during urbanization in blackbirds

Cited by 138 publications

References 55 publications

Elevated Immune Gene Expression Is Associated with Poor Reproductive Success of Urban Blue Tits

Elevated Immune Gene Expression Is Associated with Poor Reproductive Success of Urban Blue Tits

Combined epigenetic and intraspecific variation of theDRD4andSERTgenes influence novelty seeking behavior in great titParus major

Urbanization drives the evolution of parallel clines in plant populations

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