Publications by authors named "Jan T Lifjeld"

45 Publications

Sperm length variation among Afrotropical songbirds reflects phylogeny rather than adaptations to the tropical environment.

Zoology (Jena) 2020 06 23;140:125770. Epub 2020 Mar 23.

Natural History Museum, University of Oslo, P.O. Box 1172 Blindern, NO-0318 Oslo, Norway. Electronic address:

Sperm cells vary tremendously in size and shape across the animal kingdom. In songbirds (Aves: Passeri), sperm have a characteristic helical form but vary considerably in size. Most of our knowledge about sperm morphology in this group stems from studies of species in the Northern temperate zone, while little is known about the numerous species in the tropics. Here we examined sperm size in 125 Afrotropical songbird species with emphasis on the length of the major structural components (head, midpiece, flagellum), and total sperm length measured using light microscopy. Mean total sperm length varied from 51 μm to 212 μm across species. Those belonging to the Corvoidea superfamily had relatively short sperm with a small midpiece, while those of the three major Passeridan superfamilies Passeroidea, Muscicapoidea and Sylvioidea showed large interspecific variation in total sperm length and associated variation in midpiece length. These patterns are consistent with previous findings for temperate species in the same major clades. A comparative analysis with songbird species from the Northern temperate zone (N = 139) showed large overlap in sperm length ranges although certain temperate families (e.g. Parulidae, Emberizidae) typically have long sperm and certain Afrotropical families (e.g. Cisticolidae, Estrildidae) have relatively short sperm. Afrotropical and temperate species belonging to the same families showed no consistent contrasts in sperm length. Sperm length variation among Afrotropical and Northern temperate songbirds exhibits a strong phylogenetic signal with little or no evidence for any directional latitudinal effect among closely related taxa.
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http://dx.doi.org/10.1016/j.zool.2020.125770DOI Listing
June 2020

Demographic reconstruction from ancient DNA supports rapid extinction of the great auk.

Elife 2019 11 26;8. Epub 2019 Nov 26.

Department of Anatomy, University of Otago, Dunedin, New Zealand.

The great auk was once abundant and distributed across the North Atlantic. It is now extinct, having been heavily exploited for its eggs, meat, and feathers. We investigated the impact of human hunting on its demise by integrating genetic data, GPS-based ocean current data, and analyses of population viability. We sequenced complete mitochondrial genomes of 41 individuals from across the species' geographic range and reconstructed population structure and population dynamics throughout the Holocene. Taken together, our data do not provide any evidence that great auks were at risk of extinction prior to the onset of intensive human hunting in the early 16 century. In addition, our population viability analyses reveal that even if the great auk had not been under threat by environmental change, human hunting alone could have been sufficient to cause its extinction. Our results emphasise the vulnerability of even abundant and widespread species to intense and localised exploitation.
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http://dx.doi.org/10.7554/eLife.47509DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6879203PMC
November 2019

Endless forms of sexual selection.

PeerJ 2019 5;7:e7988. Epub 2019 Nov 5.

Department of Organismic and Evolutionary Biology and Museum of Comparative Zoology, Harvard University, Cambridge, MA, United States of America.

In recent years, the field of sexual selection has exploded, with advances in theoretical and empirical research complementing each other in exciting ways. This perspective piece is the product of a "stock-taking" workshop on sexual selection and sexual conflict. Our aim is to identify and deliberate on outstanding questions and to stimulate discussion rather than provide a comprehensive overview of the entire field. These questions are organized into four thematic sections we deem essential to the field. First we focus on the evolution of mate choice and mating systems. Variation in mate quality can generate both competition and choice in the opposite sex, with implications for the evolution of mating systems. Limitations on mate choice may dictate the importance of direct vs. indirect benefits in mating decisions and consequently, mating systems, especially with regard to polyandry. Second, we focus on how sender and receiver mechanisms shape signal design. Mediation of honest signal content likely depends on integration of temporally variable social and physiological costs that are challenging to measure. We view the neuroethology of sensory and cognitive receiver biases as the main key to signal form and the 'aesthetic sense' proposed by Darwin. Since a receiver bias is sufficient to both initiate and drive ornament or armament exaggeration, without a genetically correlated or even coevolving receiver, this may be the appropriate 'null model' of sexual selection. Thirdly, we focus on the genetic architecture of sexually selected traits. Despite advances in modern molecular techniques, the number and identity of genes underlying performance, display and secondary sexual traits remains largely unknown. In-depth investigations into the genetic basis of sexual dimorphism in the context of long-term field studies will reveal constraints and trajectories of sexually selected trait evolution. Finally, we focus on sexual selection and conflict as drivers of speciation. Population divergence and speciation are often influenced by an interplay between sexual and natural selection. The extent to which sexual selection promotes or counteracts population divergence may vary depending on the genetic architecture of traits as well as the covariance between mating competition and local adaptation. Additionally, post-copulatory processes, such as selection against heterospecific sperm, may influence the importance of sexual selection in speciation. We propose that efforts to resolve these four themes can catalyze conceptual progress in the field of sexual selection, and we offer potential avenues of research to advance this progress.
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http://dx.doi.org/10.7717/peerj.7988DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6839514PMC
November 2019

Extra-pair mating in a passerine bird with highly duplicated major histocompatibility complex class II: Preference for the golden mean.

Mol Ecol 2019 12 7;28(23):5133-5144. Epub 2019 Nov 7.

Natural History Museum, University of Oslo, Oslo, Norway.

Genes of the major histocompatibility complex (MHC) are essential in vertebrate adaptive immunity, and they are highly diverse and duplicated in many lineages. While it is widely established that pathogen-mediated selection maintains MHC diversity through balancing selection, the role of mate choice in shaping MHC diversity is debated. Here, we investigate female mating preferences for MHC class II (MHCII) in the bluethroat (Luscinia svecica), a passerine bird with high levels of extra-pair paternity and extremely duplicated MHCII. We genotyped family samples with mixed brood paternity and categorized their MHCII alleles according to their functional properties in peptide binding. Our results strongly indicate that females select extra-pair males in a nonrandom, self-matching manner that provides offspring with an allelic repertoire size closer to the population mean, as compared to offspring sired by the social male. This is consistent with a compatible genes model for extra-pair mate choice where the optimal allelic diversity is intermediate, not maximal. This golden mean presumably reflects a trade-off between maximizing pathogen recognition benefits and minimizing autoimmunity costs. Our study exemplifies how mate choice can reduce the population variance in individual MHC diversity and exert strong stabilizing selection on the trait. It also supports the hypothesis that extra-pair mating is adaptive through altered genetic constitution in offspring.
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http://dx.doi.org/10.1111/mec.15273DOI Listing
December 2019

Evolution of female promiscuity in Passerides songbirds.

BMC Evol Biol 2019 08 14;19(1):169. Epub 2019 Aug 14.

Natural History Museum, University of Oslo, P.O. Box 1172, Blindern, NO-0318, Oslo, Norway.

Background: Female promiscuity is highly variable among birds, and particularly among songbirds. Comparative work has identified several patterns of covariation with social, sexual, ecological and life history traits. However, it is unclear whether these patterns reflect causes or consequences of female promiscuity, or if they are byproducts of some unknown evolutionary drivers. Moreover, factors that explain promiscuity at the deep nodes in the phylogenetic tree may be different from those important at the tips, i.e. among closely related species. Here we examine the relationships between female promiscuity and a broad set of predictor variables in a comprehensive data set (N = 202 species) of Passerides songbirds, which is a highly diversified infraorder of the Passeriformes exhibiting significant variation in female promiscuity.

Results: Female promiscuity was highly variable in all major clades of the Passerides phylogeny and also among closely related species. We found several significant associations with female promiscuity, albeit with fairly small effect sizes (all R ≤ 0.08). More promiscuous species had: 1) less male parental care, particularly during the early stages of the nesting cycle (nest building and incubation), 2) more short-term pair bonds, 3) greater degree of sexual dichromatism, primarily because females were drabber, 4) more migratory behaviour, and 5) stronger pre-mating sexual selection. In a multivariate model, however, the effect of sexual selection disappeared, while the other four variables showed additive effects and together explained about 16% of the total variance in female promiscuity. Female promiscuity showed no relationship with body size, life history variation, latitude or cooperative breeding.

Conclusions: We found that multiple traits were associated with female promiscuity, but these associations were generally weak. Some traits, such as reduced parental care in males and more cryptic plumage in females, might even be responses to, rather than causes of, variation in female promiscuity. Hence, the high variation in female promiscuity among Passerides species remains enigmatic. Female promiscuity seems to be a rapidly evolving trait that often diverges between species with similar ecologies and breeding systems. A future challenge is therefore to understand what drives within-lineage variation in female promiscuity over microevolutionary time scales.
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http://dx.doi.org/10.1186/s12862-019-1493-1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6694576PMC
August 2019

Sperm head abnormalities are more frequent in songbirds with more helical sperm: A possible trade-off in sperm evolution.

J Evol Biol 2019 07 4;32(7):666-674. Epub 2019 Apr 4.

Natural History Museum, University of Oslo, Oslo, Norway.

Sperm morphology varies enormously across the animal kingdom. Whilst knowledge of the factors that drive the evolution of interspecific variation in sperm morphology is accumulating, we currently have little understanding of factors that may constrain evolutionary change in sperm traits. We investigated whether susceptibility to sperm abnormalities could represent such a constraint in songbirds, a group characterized by a distinctive helical sperm head shape. Specifically, using 36 songbird species and data from light and scanning electron microscopy, we examined among-species correlations between the occurrence of sperm head abnormalities and sperm morphology, as well as the correlation between sperm head abnormalities and two indicators of sperm competition. We found that species with more helically shaped sperm heads (i.e., a wider helical membrane and more pronounced cell waveform) had a higher percentage of abnormal sperm heads than species with less helical sperm (i.e., relatively straight sperm) and that sperm head traits were better predictors of head abnormalities than total sperm length. In contrast, there was no correlation between sperm abnormalities and the level of sperm competition. Given that songbird species with more pronounced helical sperm have higher average sperm swimming speed, our results suggest an evolutionary trade-off between sperm performance and the structural integrity of the sperm head. As such, susceptibility to morphological abnormalities may constrain the evolution of helical sperm morphology in songbirds.
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http://dx.doi.org/10.1111/jeb.13446DOI Listing
July 2019

Signatures of diversifying selection and convergence acting on passerine Toll-like receptor 4 in an evolutionary context.

Mol Ecol 2018 07 6;27(13):2871-2883. Epub 2018 Jun 6.

Department of Zoology, Faculty of Science, Charles University, Prague, Czech Republic.

Positive selection acting on Toll-like receptors (TLRs) has been recently investigated to reveal evolutionary mechanisms of host-pathogen molecular co-adaptation. Much of this research, however, has focused mainly on the identification of sites predicted to be under positive selection, bringing little insight into the functional differences and similarities among species and a limited understanding of convergent evolution in the innate immune molecules. In this study, we provide evidence of phenotypic variability in the avian TLR4 ligand-binding region (LBR), the direct interface between host and pathogen molecular structures. We show that 55 passerine species vary substantially in the distribution of electrostatic potential on the surface of the receptor, and based on these distinct patterns, we identified four species clusters. Seven of the 34 evolutionarily nonconservative and positively selected residues correspond topologically to sites previously identified as being important for lipopolysaccharide, lipid IVa or MD-2 binding. Five of these positions codetermine the identity of the charge clusters. Groups of species that host-related communities of pathogens were predicted to cluster based on their TLR4 LBR charge. Despite some evidence for convergence among taxa, there were no clear associations between the TLR4 LBR charge distribution and any of the general ecological characteristics compared (migration, latitudinal distribution and diet). Closely related species, however, mostly belonged to the same surface charge cluster indicating that phylogenetic constraints are key determinants shaping TLR4 adaptive evolution. Our results suggest that host innate immune evolution is consistent with Fahrenholz's rule on the cospeciation of hosts and their parasites.
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http://dx.doi.org/10.1111/mec.14724DOI Listing
July 2018

Genotyping strategy matters when analyzing hypervariable major histocompatibility complex-Experience from a passerine bird.

Ecol Evol 2018 02 7;8(3):1680-1692. Epub 2018 Jan 7.

Natural History Museum University of Oslo Oslo Norway.

Genotyping of classical major histocompatibility complex (MHC) genes is challenging when they are hypervariable and occur in multiple copies. In this study, we used several different approaches to genotype the moderately variable MHC class I exon 3 (MHCIe3) and the highly polymorphic MHC class II exon 2 (MHCIIβe2) in the bluethroat (). Two family groups (eight individuals) were sequenced in replicates at both markers using Ion Torrent technology with both a single- and a dual-indexed primer structure. Additionally, MHCIIβe2 was sequenced on Illumina MiSeq. Allele calling was conducted by modifications of the pipeline developed by Sommer et al. (BMC Genomics, 14, 2013, 542) and the software AmpliSAS. While the different genotyping strategies gave largely consistent results for MHCIe3, with a maximum of eight alleles per individual, MHCIIβe2 was remarkably complex with a maximum of 56 MHCIIβe2 alleles called for one individual. Each genotyping strategy detected on average 50%-82% of all MHCIIβe2 alleles per individual, but dropouts were largely allele-specific and consistent within families for each strategy. The discrepancies among approaches indicate PCR biases caused by the platform-specific primer tails. Further, AmpliSAS called fewer alleles than the modified Sommer pipeline. Our results demonstrate that allelic dropout is a significant problem when genotyping the hypervariable MHCIIβe2. As these genotyping errors are largely nonrandom and method-specific, we caution against comparing genotypes across different genotyping strategies. Nevertheless, we conclude that high-throughput approaches provide a major advance in the challenging task of genotyping hypervariable MHC loci, even though they may not reveal the complete allelic repertoire.
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http://dx.doi.org/10.1002/ece3.3757DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5792522PMC
February 2018

Is telomere length associated with mate choice in a songbird with a high rate of extra-pair paternity?

PLoS One 2017 4;12(8):e0182446. Epub 2017 Aug 4.

Department of Biological and Environmental Sciences, University of Gothenburg, Gothenburg, Sweden.

Telomere length is related to aging in many eukaryotes and the rate of telomere attrition has been suggested to reflect individual genetic quality. Telomere length could thus have implications for mate choice. We investigated telomere length variation in bluethroat Luscinia svecica families with mixed paternity, including social parents, extra-pair fathers and nestlings, testing whether telomere length is associated with social and/or extra-pair mate choice through assortative mating or selection of mates with relatively long telomeres. In adults, relative telomere length (rTL) did not differ between the sexes, nor between two age categories. In chicks, however, rTL decreased with body mass at sampling (an index of nestling age). We found a positive correlation between the rTL of social mates, suggesting assortative mating with respect to telomere length or a correlative thereof. However, extra-pair males did not differ from social mates in rTL, and accordingly there was also no difference between within- and extra-pair young (i.e. half-siblings) when controlling for the effect of mass. We found no relationships between telomere length, age and fitness-related traits in adults, but an intriguing year-difference in telomere length in both sexes. In conclusion, we found no support for the idea that females choose extra-pair males based on their telomere length, but social mate choice seems to be influenced by rTL, possibly through its co-variation with aspects reflecting individual quality, like early arrival at the breeding grounds.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0182446PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5544213PMC
October 2017

Complete mitochondrial genomes of eleven extinct or possibly extinct bird species.

Mol Ecol Resour 2017 Mar 11;17(2):334-341. Epub 2016 Oct 11.

Natural History Museum, University of Oslo, PO Box 1172 Blindern, Oslo, 0318, Norway.

Natural history museum collections represent a vast source of ancient and historical DNA samples from extinct taxa that can be utilized by high-throughput sequencing tools to reveal novel genetic and phylogenetic information about them. Here, we report on the successful sequencing of complete mitochondrial genome sequences (mitogenomes) from eleven extinct bird species, using de novo assembly of short sequences derived from toepad samples of degraded DNA from museum specimens. For two species (the Passenger Pigeon Ectopistes migratorius and the South Island Piopio Turnagra capensis), whole mitogenomes were already available from recent studies, whereas for five others (the Great Auk Pinguinis impennis, the Imperial Woodpecker Campehilus imperialis, the Huia Heteralocha acutirostris, the Kauai Oo Moho braccathus and the South Island Kokako Callaeas cinereus), there were partial mitochondrial sequences available for comparison. For all seven species, we found sequence similarities of >98%. For the remaining four species (the Kamao Myadestes myadestinus, the Paradise Parrot Psephotellus pulcherrimus, the Ou Psittirostra psittacea and the Lesser Akialoa Akialoa obscura), there was no sequence information available for comparison, so we conducted blast searches and phylogenetic analyses to determine their phylogenetic positions and identify their closest extant relatives. These mitogenomes will be valuable for future analyses of avian phylogenetics and illustrate the importance of museum collections as repositories for genomics resources.
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http://dx.doi.org/10.1111/1755-0998.12600DOI Listing
March 2017

Sperm performance in conspecific and heterospecific female fluid.

Ecol Evol 2016 Mar 30;6(5):1363-77. Epub 2016 Jan 30.

Natural History Museum University of Oslo PO Box 1172 Blindern 0318 Oslo Norway.

Divergent sexual selection within allopatric populations may result in divergent sexual phenotypes, which can act as reproductive barriers between populations upon secondary contact. This hypothesis has been most tested on traits involved in precopulatory sexual selection, with less work focusing on traits that act after copulation and before fertilization (i.e., postcopulatory prezygotic traits), particularly in internally fertilizing vertebrates. However, postcopulatory sexual selection within species can also drive trait divergence, resulting in reduced performance of heterospecific sperm within the female reproductive tract. Such incompatibilities, arising as a by-product of divergent postcopulatory sexual selection in allopatry, can represent reproductive barriers, analogous to species-assortative mating preferences. Here, we tested for postcopulatory prezygotic reproductive barriers between three pairs of taxa with diverged sperm phenotypes and moderate-to-high opportunity for postcopulatory sexual selection (barn swallows Hirundo rustica versus sand martins Riparia riparia, two subspecies of bluethroats, Luscinia svecica svecica versus L. s. namnetum, and great tits Parus major versus blue tits Cyanistes caeruleus). We tested sperm swimming performance in fluid from the outer reproductive tract of females, because the greatest reduction in sperm number in birds occurs as sperm swim across the vagina. Contrary to our expectations, sperm swam equally well in fluid from conspecific and heterospecific females, suggesting that postcopulatory prezygotic barriers do not act between these taxon pairs, at this stage between copulation and fertilization. We therefore suggest that divergence in sperm phenotypes in allopatry is insufficient to cause widespread postcopulatory prezygotic barriers in the form of impaired sperm swimming performance in passerine birds.
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http://dx.doi.org/10.1002/ece3.1977DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4733106PMC
March 2016

When taxonomy meets genomics: lessons from a common songbird.

Authors:
Jan T Lifjeld

Mol Ecol 2015 Jun;24(12):2901-3

Natural History Museum, University of Oslo, PO Box 1172, Blindern, 0318, Oslo, Norway.

Taxonomy is being increasingly informed by genomics. Traditionally, taxonomy has relied extensively on phenotypic traits for the identification and delimitation of species, though with a growing influence from molecular phylogenetics in recent decades. Now, genomics opens up new and more powerful tools for analysing the evolutionary history and relatedness among species, as well as understanding the genetic basis for phenotypic traits and their role in reproductive isolation. New insights gained from genomics will therefore have major effects on taxonomic classifications and species delimitation. How a genomics approach can inform a flawed taxonomy is nicely exemplified by Mason & Taylor () in this issue of Molecular Ecology. They studied redpolls, which comprise a genus (Acanthis) of fringillid finches with a wide distribution in the Holarctic region, and whose species taxonomy has been a matter of much controversy for decades (Fig. ). Current authoritative checklists classify them into one, two or three species, and five or six subspecies, based largely on geographical differences in phenotypic traits. Previous studies, including a recent one of the subspecies on Iceland (Amouret et al. ), have found no evidence of differentiation between these taxa in conventional molecular markers. The lack of genetic structure has been interpreted as incomplete lineage sorting among rapidly evolving lineages. Now Mason & Taylor (), using a large data set of genomewide SNPs, verify that they all belong to a single gene pool with a common evolutionary history, and with little or no geographical structuring. They also show that phenotypic traits used in taxonomic classifications (plumage and bill morphology) are closely associated with polygenic patterns of gene expression, presumably driven by ecological selection on a few regulatory genes. Several lessons can be learned from this study. Perhaps the most important one for taxonomy is the risk of taxonomic inflation resulting from overemphasizing phenotypic traits under local adaptation and ignoring a lack of phylogenetic signal in molecular markers.
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http://dx.doi.org/10.1111/mec.13244DOI Listing
June 2015

Commonness and ecology, but not bigger brains, predict urban living in birds.

BMC Ecol 2015 Apr 11;15:12. Epub 2015 Apr 11.

Natural History Museum, University of Oslo, P.O. Box 1172 Blindern, NO-0318, Oslo, Norway.

Background: Several life history and ecological variables have been reported to affect the likelihood of species becoming urbanized. Recently, studies have also focused on the role of brain size in explaining ability to adapt to urban environments. In contrast, however, little is known about the effect of colonization pressure from surrounding areas, which may confound conclusions about what makes a species urban. We recorded presence/absence data for birds in 93 urban sites in Oslo (Norway) and compared these with species lists generated from 137 forest and 51 farmland sites surrounding Oslo which may represent source populations for colonization.

Results: We found that the frequency (proportion of sites where present) of a species within the city was strongly and positively associated with its frequency in sites surrounding the city, as were both species breeding habitat and nest site location. In contrast, there were generally no significant effects of relative brain mass or migration on urban occupancy. Furthermore, analyses of previously published data showed that urban density of birds in six other European cities was also positively and significantly associated with density in areas outside cities, whereas relative brain mass showed no such relationship.

Conclusions: These results suggest that urban bird communities are primarily determined by how frequently species occurred in the surrounding landscapes and by features of ecology (i.e. breeding habitat and nest site location), whereas species' relative brain mass had no significant effects.
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http://dx.doi.org/10.1186/s12898-015-0044-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4412207PMC
April 2015

Postcopulatory sexual selection is associated with accelerated evolution of sperm morphology.

Evolution 2015 Apr 21;69(4):1044-52. Epub 2015 Mar 21.

Natural History Museum, University of Oslo, PO Box 1172, Blindern, 0318, Oslo, Norway; Centre for Ecological and Evolutionary Synthesis, Department of Biosciences, University of Oslo, PO Box 1066, Blindern, 0316, Oslo, Norway.

Rapid diversification of sexual traits is frequently attributed to sexual selection, though explicit tests of this hypothesis remain limited. Spermatozoa exhibit remarkable variability in size and shape, and studies report a correlation between sperm morphology (sperm length and shape) and sperm competition risk or female reproductive tract morphology. However, whether postcopulatory processes (e.g., sperm competition and cryptic female choice) influence the speed of evolutionary diversification in sperm form is unknown. Using passerine birds, we quantified evolutionary rates of sperm length divergence among lineages (i.e., species pairs) and determined whether these rates varied with the level of sperm competition (estimated as relative testes mass). We found that relative testes mass was significantly and positively associated with more rapid phenotypic divergence in sperm midpiece and flagellum lengths, as well as total sperm length. In contrast, there was no association between relative testes mass and rates of evolutionary divergence in sperm head size, and models suggested that head length is evolutionarily constrained. Our results are the first to show an association between the strength of sperm competition and the speed of sperm evolution, and suggest that postcopulatory sexual selection promotes rapid evolutionary diversification of sperm morphology.
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http://dx.doi.org/10.1111/evo.12620DOI Listing
April 2015

Morphology-function relationships and repeatability in the sperm of Passer sparrows.

J Morphol 2015 Apr 26;276(4):370-7. Epub 2014 Nov 26.

Natural History Museum, University of Oslo, Blindern, 0318, Oslo, Norway.

Sperm performance is likely to be an important determinant of male reproductive success, especially when females copulate with multiple males. Understanding sperm performance is therefore crucial to fully understand the evolution of male reproductive strategies. In this study, we examined the repeatability of sperm morphology and motility measures over three breeding seasons, and we studied relationships between sperm morphology and function. We conducted this study in wild-derived captive house sparrows (Passer domesticus) and Spanish sparrows (P. hispaniolensis). Results for the two species were similar. As predicted from results in other passerine species, total sperm length was highly repeatable across ejaculates, and repeatability for the length of other components was moderate. The repeatability of sperm swimming speed across ejaculates was lower, but statistically significant, suggesting that sperm velocity may be a relatively dynamic trait. Surprisingly, swimming speed did not correlate with the relative length of the midpiece, and it correlated negatively with the relative length of the flagellum and with total sperm length. This pattern is the opposite of what theory predicts and differs from what has been found in house sparrows before. Also contrary to previous work, we found no evidence that total sperm length correlates with sperm longevity. These results therefore highlight the need for a better understanding of relationships between sperm morphology and function in passerine birds.
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http://dx.doi.org/10.1002/jmor.20346DOI Listing
April 2015

The evolutionary history of Afrocanarian blue tits inferred from genomewide SNPs.

Mol Ecol 2015 Jan 3;24(1):180-91. Epub 2014 Dec 3.

University Museum of Bergen, P.O. Box 7800, 5007, Bergen, Norway.

A common challenge in phylogenetic reconstruction is to find enough suitable genomic markers to reliably trace splitting events with short internodes. Here, we present phylogenetic analyses based on genomewide single-nucleotide polymorphisms (SNPs) of an enigmatic avian radiation, the subspecies complex of Afrocanarian blue tits (Cyanistes teneriffae). The two sister species, the Eurasian blue tit (Cyanistes caeruleus) and the azure tit (Cyanistes cyanus), constituted the out-group. We generated a large data set of SNPs for analysis of population structure and phylogeny. We also adapted our protocol to utilize degraded DNA from old museum skins from Libya. We found strong population structuring that largely confirmed subspecies monophyly and constructed a coalescent-based phylogeny with full support at all major nodes. The results are consistent with a recent hypothesis that La Palma and Libya are relic populations of an ancient Afrocanarian blue tit, although a small data set for Libya could not resolve its position relative to La Palma. The birds on the eastern islands of Fuerteventura and Lanzarote are similar to those in Morocco. Together they constitute the sister group to the clade containing the other Canary Islands (except La Palma), in which El Hierro is sister to the three central islands. Hence, extant Canary Islands populations seem to originate from multiple independent colonization events. We also found population divergences in a key reproductive trait, viz. sperm length, which may constitute reproductive barriers between certain populations. We recommend a taxonomic revision of this polytypic species, where several subspecies should qualify for species rank.
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http://dx.doi.org/10.1111/mec.13008DOI Listing
January 2015

Allelic variation in a willow warbler genomic region is associated with climate clines.

PLoS One 2014 1;9(5):e95252. Epub 2014 May 1.

Department of Biology, Centre for Animal Movement Research, Ecology Building, Lund University, Lund, Sweden.

Local adaptation is an important process contributing to population differentiation which can occur in continuous or isolated populations connected by various amounts of gene flow. The willow warbler (Phylloscopus trochilus) is one of the most common songbirds in Fennoscandia. It has a continuous breeding distribution where it is found in all forested habitats from sea level to the tree line and therefore constitutes an ideal species for the study of locally adapted genes associated with environmental gradients. Previous studies in this species identified a genetic marker (AFLP-WW1) that showed a steep north-south cline in central Sweden with one allele associated with coastal lowland habitats and the other with mountainous habitats. It was further demonstrated that this marker is embedded in a highly differentiated chromosome region that spans several megabases. In the present study, we sampled 2,355 individuals at 128 sites across all of Fennoscandia to study the geographic and climatic variables associated with the allele frequency distributions of WW1. Our results demonstrate that 1) allele frequency patterns significantly differ between mountain and lowland populations, 2) these allele differences coincide with extreme temperature conditions and the short growing season in the mountains, and milder conditions in coastal areas, and 3) the northern-allele or "altitude variant" of WW1 occurs in willow warblers that occupy mountainous habitat regardless of subspecies. Finally these results suggest that climate may exert selection on the genomic region associated with these alleles and would allow us to develop testable predictions for the distribution of the genetic marker based on climate change scenarios.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0095252PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4006793PMC
December 2014

Promiscuity, sexual selection, and genetic diversity: a reply to Spurgin.

Evolution 2013 Oct 13;67(10):3073-4. Epub 2013 Aug 13.

Natural History Museum, University of Oslo, 0318, Oslo, Norway.

We recently reported a positive association between female promiscuity and genetic diversity across passerine birds, and launched the hypothesis that female promiscuity acts as a balancing selection, pressure maintaining genetic diversity in populations (Gohli et al.2013). Spurgin (2013) questions both our analyses and interpretations. While we agree that the hypothesis needs more comprehensive empirical testing, we find his specific points of criticism unjustified. In a more general perspective, we call for a more explicit recognition of female mating preferences as mechanisms of selection in population genetics theory.
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http://dx.doi.org/10.1111/evo.12211DOI Listing
October 2013

Patterns of sperm damage in Chernobyl passerine birds suggest a trade-off between sperm length and integrity.

Biol Lett 2013 Oct 2;9(5):20130530. Epub 2013 Oct 2.

Departamento de Anatomía, Biología Celular y Zoología, Universidad de Extremadura, , Avenida de Elvas s/n, 06071 Badajoz, Spain.

Interspecific variation in sperm size is enigmatic, but generally assumed to reflect species-specific trade-offs in selection pressures. Among passerine birds, sperm length varies sevenfold, and sperm competition risk seems to drive the evolution of longer sperm. However, little is known about factors favouring short sperm or constraining the evolution of longer sperm. Here, we report a comparative analysis of sperm head abnormalities among 11 species of passerine bird in Chernobyl, presumably resulting from chronic irradiation following the 1986 accident. Frequencies of sperm abnormalities varied between 15.7 and 77.3% among species, more than fourfold higher than in uncontaminated areas. Nonetheless, species ranked similarly in sperm abnormalities in unpolluted areas as in Chernobyl, pointing to intrinsic factors underlying variation in sperm damage among species. Scanning electron microscopy of abnormal spermatozoa revealed patterns of acrosome damage consistent with premature acrosome reaction. Sperm length, but not sperm competition risk explained variation in sperm damage among species. This suggests that longer spermatozoa are more susceptible to premature acrosome reaction. Therefore, we hypothesize a trade-off between sperm length and sperm integrity affecting sperm evolution in passerine birds.
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http://dx.doi.org/10.1098/rsbl.2013.0530DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3971692PMC
October 2013

Female promiscuity is positively associated with neutral and selected genetic diversity in passerine birds.

Evolution 2013 May 23;67(5):1406-19. Epub 2013 Jan 23.

National Centre for Biosystematics, Natural History Museum, University of Oslo, 0318 Oslo, Norway.

Passerine birds show large interspecific variation in extrapair paternity rates. There is accumulating evidence that such promiscuous behavior is driven by indirect, genetic benefits to females. Sexual selection theory distinguishes between two types of genetic benefits, additive and nonadditive effects, mediated by preferences for good and compatible genes, respectively. Good genes preferences should imply directional selection and mating skew among males, and thus reduced genetic diversity in the population. In contrast, compatible genes preferences should give balancing selection that retains genetic diversity. Here, we test how well these predictions fit with patterns of variation in genetic diversity and promiscuity levels among passerine birds. We found that more promiscuous species had higher nucleotide diversity at autosomal introns, but not at Z-chromosome introns. We also found that major histocompatibility complex (MHC) class IIB alleles had higher sequence diversity, and therefore should recognize a broader spectrum of pathogens, in more promiscuous species. Our results suggest that female promiscuity targets a multitude of autosomal genes for their nonadditive, compatibility benefits. Also, as immunity genes seem to be of particular importance, we hypothesize that interspecific variation in female promiscuity among passerine birds has arisen in response to the strength of pathogen-mediated selection.
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http://dx.doi.org/10.1111/evo.12045DOI Listing
May 2013

Deep sympatric mtDNA divergence in the autumnal moth (Epirrita autumnata).

Ecol Evol 2012 Jan 14;3(1):126-44. Epub 2012 Dec 14.

Natural History Museum, University of Oslo P.O. Box 1172, Blindern, N-0318, Oslo, Norway ; Department of Basic Sciences and Aquatic Medicine, Norwegian School of Veterinary Science P.O. Box 8146 Dep, N-0033, Oslo, Norway.

Deep sympatric intraspecific divergence in mtDNA may reflect cryptic species or formerly distinct lineages in the process of remerging. Preliminary results from DNA barcoding of Scandinavian butterflies and moths showed high intraspecific sequence variation in the autumnal moth, Epirrita autumnata. In this study, specimens from different localities in Norway and some samples from Finland and Scotland, with two congeneric species as outgroups, were sequenced with mitochondrial and nuclear markers to resolve the discrepancy found between mtDNA divergence and present species-level taxonomy. We found five COI sub-clades within the E. autumnata complex, most of which were sympatric and with little geographic structure. Nuclear markers (ITS2 and Wingless) showed little variation and gave no indications that E. autumnata comprises more than one species. The samples were screened with primers for Wolbachia outer surface gene (wsp) and 12% of the samples tested positive. Two Wolbachia strains were associated with different mtDNA sub-clades within E. autumnata, which may indicate indirect selection/selective sweeps on haplotypes. Our results demonstrate that deep mtDNA divergences are not synonymous with cryptic speciation and this has important implications for the use of mtDNA in species delimitation, like in DNA barcoding.
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http://dx.doi.org/10.1002/ece3.434DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3568849PMC
January 2012

Deep sympatric mitochondrial divergence without reproductive isolation in the common redstart Phoenicurus phoenicurus.

Ecol Evol 2012 Dec 2;2(12):2974-88. Epub 2012 Nov 2.

National Centre for Biosystematics, Natural History Museum, University of Oslo P.O. Box 1172, Blindern, NO-0318, Oslo, Norway.

Mitochondrial DNA usually shows low sequence variation within and high sequence divergence among species, which makes it a useful marker for phylogenetic inference and DNA barcoding. A previous study on the common redstart (Phoenicurus phoenicurus) revealed two very different mtDNA haplogroups (5% K2P distance). This divergence is comparable to that among many sister species; however, both haplogroups coexist and interbreed in Europe today. Herein, we describe the phylogeographic pattern of these lineages and test hypotheses for how such high diversity in mtDNA has evolved. We found no evidence for mitochondrial pseudogenes confirming that both haplotypes are of mitochondrial origin. When testing for possible reproductive barriers, we found no evidence for lineage-specific assortative mating and no difference in sperm morphology, indicating that they are not examples of cryptic species, nor likely to reflect the early stages of speciation. A gene tree based on a short fragment of cytochrome c oxidase subunit 1 from the common redstart and 10 other Phoenicurus species, showed no introgression from any of the extant congenerics. However, introgression from an extinct congeneric cannot be excluded. Sequences from two nuclear introns did not show a similar differentiation into two distinct groups. Mismatch distributions indicated that the lineages have undergone similar demographic changes. Taken together, these results confirm that deeply divergent mitochondrial lineages can coexist in biological species. Sympatric mtDNA divergences are relatively rare in birds, but the fact that they occur argues against the use of threshold mtDNA divergences in species delineation.
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http://dx.doi.org/10.1002/ece3.398DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3538993PMC
December 2012

Evolution of sperm structure and energetics in passerine birds.

Proc Biol Sci 2013 Feb 2;280(1753):20122616. Epub 2013 Jan 2.

Natural History Museum, University of Oslo, 0318 Oslo, Norway.

Spermatozoa exhibit considerable interspecific variability in size and shape. Our understanding of the adaptive significance of this diversity, however, remains limited. Determining how variation in sperm structure translates into variation in sperm performance will contribute to our understanding of the evolutionary diversification of sperm form. Here, using data from passerine birds, we test the hypothesis that longer sperm swim faster because they have more available energy. We found that sperm with longer midpieces have higher levels of intracellular adenosine triphosphate (ATP), but that greater energy reserves do not translate into faster-swimming sperm. Additionally, we found that interspecific variation in sperm ATP concentration is not associated with the level of sperm competition faced by males. Finally, using Bayesian methods, we compared the evolutionary trajectories of sperm morphology and ATP content, and show that both traits have undergone directional evolutionary change. However, in contrast to recent suggestions in other taxa, we show that changes in ATP are unlikely to have preceded changes in morphology in passerine sperm. These results suggest that variable selective pressures are likely to have driven the evolution of sperm traits in different taxa, and highlight fundamental biological differences between taxa with internal and external fertilization, as well as those with and without sperm storage.
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http://dx.doi.org/10.1098/rspb.2012.2616DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3574354PMC
February 2013

Sperm competition in tropical versus temperate zone birds.

Proc Biol Sci 2013 Feb 12;280(1752):20122434. Epub 2012 Dec 12.

Institute of Vertebrate Biology, vvi, Academy of Sciences of the Czech Republic, Kvetna 8, Brno 603 65, Czech Republic.

Sperm competition represents an important component of post-copulatory sexual selection. It has been argued that the level of sperm competition declines in birds towards the equator. However, to date, sperm competition estimates have been available mainly for avian species inhabiting the northern temperate zone. Here we apply a novel approach, using the coefficient of between-male variation (CV(bm)) in sperm size as an index for sperm competition risk, in a comparative analysis of 31 Afrotropical and 99 northern temperate zone passerine species. We found no difference in sperm competition risk between the two groups, nor any relationship with migration distance. However, a multivariate model indicated that sperm competition risk was highest in species with a combination of low body mass and few eggs per clutch. The effect of clutch size was most pronounced in tropical species, which indicates that sperm competition risk in tropical and temperate species is differently associated with particular life-history traits. Although tropical species had lower sperm competition risk than temperate zone species for overlapping clutch sizes, the idea of a generally reduced risk of sperm competition in tropical birds was not supported by our analysis.
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http://dx.doi.org/10.1098/rspb.2012.2434DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3574308PMC
February 2013

No evidence for pre-copulatory sexual selection on sperm length in a passerine bird.

PLoS One 2012 27;7(2):e32611. Epub 2012 Feb 27.

Natural History Museum, National Centre for Biosystematics, University of Oslo, Oslo, Norway.

There is growing evidence that post-copulatory sexual selection, mediated by sperm competition, influences the evolution of sperm phenotypes. Evidence for pre-copulatory sexual selection effects on sperm traits, on the other hand, is rather scarce. A recent paper on the pied flycatcher, Ficedula hypoleuca, reported phenotypic associations between sperm length and two sexually selected male traits, i.e. plumage colour and arrival date, thus invoking pre-copulatory sexual selection for longer sperm. We were unable to replicate these associations with a larger data set from the same and two additional study populations; sperm length was not significantly related to either male plumage colour or arrival date. Furthermore, there was no significant difference in sperm length between populations despite marked differences in male plumage colour. We also found some evidence against the previously held assumption of longer sperm being qualitatively superior; longer sperm swam at the same speed as shorter sperm, but were less able to maintain speed over time. We argue that both empirical evidence and theoretical considerations suggest that the evolution of sperm morphology is not primarily associated with pre-copulatory sexual selection on male secondary sexual traits in this or other passerine bird species. The relatively large between-male variation in sperm length in this species is probably due to relaxed post-copulatory sexual selection.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0032611PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3287978PMC
August 2012

Age before beauty? Relationships between fertilization success and age-dependent ornaments in barn swallows.

Behav Ecol Sociobiol 2011 Sep 22;65(9):1687-1697. Epub 2011 Mar 22.

When males become more ornamented and reproduce more successfully as they grow older, phenotypic correlations between ornament exaggeration and reproductive success can be confounded with age effects in cross-sectional studies, and thus say relatively little about sexual selection on these traits. This is exemplified here in a correlative study of male fertilization success in a large colony of American barn swallows (Hirundo rustica erythrogaster). Previous studies of this species have indicated that two sexually dimorphic traits, tail length and ventral plumage coloration, are positively correlated with male fertilization success, and a mechanism of sexual selection by female choice has been invoked. However, these studies did not control for potential age-related variation in trait expression. Here, we show that male fertilization success was positively correlated with male tail length but not with plumage coloration. We also show that 1-year-old males had shorter tails and lower fertilization success than older males. This age effect accounted for much of the covariance between tail length and fertilization success. Still, there was a positive relationship between tail length and fertilization success among older males. But as this group consisted of males from different age classes, an age effect may be hidden in this relationship as well. Our data also revealed a longitudinal increase in both tail length and fertilization success for individual males. We argue that age-dependent ornament expression and reproductive performance in males complicate inferences about female preferences and sexual selection.
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http://dx.doi.org/10.1007/s00265-011-1176-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3156913PMC
September 2011

Factors affecting germline mutations in a hypervariable microsatellite: a comparative analysis of six species of swallows (Aves: Hirundinidae).

Mutat Res 2011 Mar 1;708(1-2):37-43. Epub 2011 Feb 1.

National Centre for Biosystematics, Natural History Museum, University of Oslo, P.O. Box 1172 Blindern, NO-0318 Oslo, Norway.

Microsatellites mutate frequently by replication slippage. Empirical evidence shows that the probability of such slippage mutations may increase with the length of the repeat region as well as exposure to environmental mutagens, but the mutation rate can also differ between the male and female germline. It has been hypothesized that more intense sexual selection or sperm competition can also lead to elevated mutation rates, but the empirical evidence is inconclusive. Here, we analyzed the occurrence of germline slippage mutations in the hypervariable pentanucleotide microsatellite locus HrU10 across six species of swallow (Aves: Hirundinidae). These species exhibit marked differences in the length range of the microsatellite, as well as differences in the intensity of sperm competition. We found a strong effect of microsatellite length on the probability of mutation, but no residual effect of species or their level of sperm competition when the length effect was accounted for. Neither could we detect any difference in mutation rate between tree swallows (Tachycineta bicolor) breeding in Hamilton Harbour, Ontario, an industrial site with previous documentation of elevated mutation rates for minisatellite DNA, and a rural reference population. However, our cross-species analysis revealed two significant patterns of sex differences in HrU10 germline mutations: (1) mutations in longer alleles occurred typically in the male germline, those in shorter alleles in the female germline, and (2) male germline mutations were more often expansions than contractions, whereas no directional bias was evident in the female germline. These results indicate some fundamental differences in male and female gametogenesis affecting the probability of slippage mutations. Our study also reflects the value of a comparative, multi-species approach for locus-specific mutation analyses, through which a wider range of influential factors can be assessed than in single-species studies.
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http://dx.doi.org/10.1016/j.mrfmmm.2011.01.006DOI Listing
March 2011

Sperm length variation as a predictor of extrapair paternity in passerine birds.

PLoS One 2010 Oct 18;5(10):e13456. Epub 2010 Oct 18.

National Centre for Biosystematics, Natural History Museum, University of Oslo, Oslo, Norway.

Background: The rate of extrapair paternity is a commonly used index for the risk of sperm competition in birds, but paternity data exist for only a few percent of the approximately 10400 extant species. As paternity analyses require extensive field sampling and costly lab work, species coverage in this field will probably not improve much in the foreseeable future. Recent findings from passerine birds, which constitute the largest avian order (∼5,900 species), suggest that sperm phenotypes carry a signature of sperm competition. Here we examine how well standardized measures of sperm length variation can predict the rate of extrapair paternity in passerine birds.

Methodology/principal Findings: We collected sperm samples from 55 passerine species in Canada and Europe for which extrapair paternity rates were already available from either the same (n = 24) or a different (n = 31) study population. We measured the total length of individual spermatozoa and found that both the coefficient of between-male variation (CV(bm)) and within-male variation (CV(wm)) in sperm length were strong predictors of the rate of extrapair paternity, explaining as much as 65% and 58%, respectively, of the variation in extrapair paternity among species. However, only the CV(bm) predictor was independent of phylogeny, which implies that it can readily be converted into a currency of extrapair paternity without the need for phylogenetic correction.

Conclusion/significance: We propose the CV(bm) index as an alternative measure to extrapair paternity for passerine birds. Given the ease of sperm extraction from male birds in breeding condition, and a modest number of sampled males required for a robust estimate, this new index holds a great potential for mapping the risk of sperm competition across a wide range of passerine birds.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0013456PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2956655PMC
October 2010

Identification of blood parasites in old world warbler species from the Danube River Delta.

Avian Dis 2009 Dec;53(4):634-6

Department of Zoology and Laboratory of Ornithology, Faculty of Science, Palacky University, Tr. Svobody 26, CZ-771 46 Olomouc, Czech Republic.

Warbler species of the families Sylviidae and Acrocephalidae occurring in the Danube river delta are frequently exposed to blood-sucking arthropods that transmit avian blood parasites. We investigated infections by three genera of hemosporidian parasites in blood samples from six warbler species. Altogether in 17 (32.6%) of 52 blood samples, a PCR product was amplified. The great reed warbler (Acrocephalus arundinaceus) had the highest prevalence, with 63.6% (7/11) infected individuals, whereas no infection was detected in marsh warbler (Acrocephalus palustris). The most common parasite genus was Haemoproteus, which was found in 15.4% (8/52) of individuals. Seven known parasite lineages (five Haemoproteus and two Plasmodium) and two new lineages were recorded (one Leucocytozoon and one Plasmodium).
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http://dx.doi.org/10.1637/8842-040409-Case.1DOI Listing
December 2009

The use of blue tit eggs as a biomonitoring tool for organohalogenated pollutants in the European environment.

Sci Total Environ 2010 Feb 13;408(6):1451-7. Epub 2010 Jan 13.

Laboratory of Ethology, Department of Biology, University of Antwerp, Universiteitsplein 1, Wilrijk, Belgium.

In the present study, large scale geographical variation in the occurrence of organohalogenated pollutants (OHPs) was investigated throughout Europe using eggs of a terrestrial resident passerine species, the blue tit (Cyanistes caeruleus). Blue tit eggs from 10 sampling locations, involving suburban, rural and remote areas, in 7 European countries were collected and analysed. Sum polychlorinated biphenyl (PCB) levels ranged from 150ng/g lipid weight (lw) to 2003ng/g lw. Sum polybrominated diphenyl ethers (PBDEs) ranged from 3.95ng/g lw to 114ng/g lw. As expected, PCB and PBDE concentrations were significantly higher in the sampled suburban locations compared to the rural and remote locations. Sum organochlorine pesticides (OCPs) ranged from 122ng/g lw to 775ng/g lw. OCP concentrations were, against the expectations, found to be lower in the rural sampling locations compared to the other locations. Contamination profiles of PCBs, PBDEs and OCPs differed also among the sampling locations, which may be due to local contamination sources. Finally, we compared the results of this study with previously reported OHP concentrations in the eggs of a closely related species, the great tit (Parus major), from the same sampling locations in Europe. We found no differences in concentrations between the species. In addition, we found a significant, positive correlation between the sum PCB concentrations in blue tit eggs and great tit eggs, suggesting similar exposure pathways, mechanisms of accumulation and maternal transfer of PCBs. In conclusion, our results suggest the usefulness of eggs from passerine birds as a biomonitoring tool for OHPs on a large geographical scale.
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http://dx.doi.org/10.1016/j.scitotenv.2009.12.028DOI Listing
February 2010