Phylogeography of the blue tit ( Parus teneriffae -group) on the Canary Islands based on mitochondrial DNA sequence data and morphometrics

An analysis of the sequences of the mitochondrial cytochrome b gene (1005 bp) of the Parus teneriffae-group from the Canary Islands and North Africa revealed new insights into the phylogeography of this taxon. The origin of the radiation on the Canarian Archipelago was apparently one of the central islands—Tenerife or Gran Canaria. The populations on El Hierro (P. t. ombriosus) and La Palma (P. t. palmensis) represent distinct monophyletic lineages. Blue tits from Gran Canaria are genetically distinct from those of La Gomera and Tenerife (P. t. teneriffae), which supports the results of other studies and suggests the existence of an—until now—undescribed taxon there. In contrast, the populations on the eastern islands of Fuerteventura and Lanzarote (P. t. degener) could not be distinguished from North African blue tits (P. t. ultramarinus), and these populations should be subsumed under the subspecies ultramarinus. Taxonomic recommendations based on these results include the distinction of the northern European P. caeruleus from P. teneriffae, including blue tits from North Africa and the Canary Islands, the treatment of degener and ultramarinus as synonymous (P. teneriffae ultramarinus) and a new blue tit taxon on the island of Gran Canaria (P. t. hedwigii nov. ssp.), which is formally described. The genetic results are in parts supported by bioacoustic and morphological data.     

A multi-gene approach reveals a complex evolutionary history in the Cyanistes species group

Quaternary climatic oscillations have been considered decisive in shaping much of the phylogeographic structure around the Mediterranean Basin. Within this paradigm, peripheral islands are usually considered as the endpoints of the colonization processes. Here, we use nuclear and mitochondrial markers to investigate the phylogeography of the blue tit complex (blue tit Cyanistes caeruleus, Canary blue tit C. teneriffae and azure tit C. cyanus), and assess the role of the Canary Islands for the geographic structuring of genetic variation. The Canary blue tit exhibits strong genetic differentiation within the Canary Islands and, in combination with other related continental species, provides an ideal model in which to examine recent differentiation within a closely related group of continental and oceanic island avian species. We analysed DNA sequences from 51 breeding populations and more than 400 individuals in the blue tit complex. Discrepancies in the nuclear and mitochondrial gene trees provided evidence of a complex evolutionary process around the Mediterranean Basin. Coalescent analyses revealed gene flow between C. caeruleus and C. teneriffae suggesting a dynamic process with multiple phases of colonization and geographic overlapping ranges. Microsatellite data indicated strong genetic differentiation among the Canary Islands and between the Canary archipelago and the close continental areas, indicating limited contemporary gene flow. Diversification of the blue tit complex is estimated to have started during the early Pliocene (≈ 5 Ma), coincident with the end of Messinian salinity crisis. Phylogenetic analyses indicated that the North African blue tit is derived from the Canary blue tits, a pattern is avian 'back colonization' that contrasts with more traditionally held views of islands being sinks rather than sources.     

Colonization and diversification of the species Brachyderes rugatus (Coleoptera) on the Canary Islands: evidence from mitochondrial DNA COII gene sequences

Abstract.— The genus Brachyderes Schönherr (Coleoptera: Curculionidae) is represented by the species B. rugatus Wollaston on the Canary Islands, with one subspecies on each of the islands of Gran Canaria, Tenerife, La Palma, and El Hierro. These four subspecies are associated with the endemic pine tree Pinus canariensis , and their distributions are broadly coincident. Eighty-eight individual Canarian Brachyderes , sampled from across the distributions of each subspecies, have been sequenced for 570 bp of the mitochondrial DNA (mtDNA) cytochrome oxidase II gene (COII). No mitotypes are shared among islands. Both maximum-likelihood and distance-based phylogenetic analyses have shown that: Tenerife is composed of a single monophyletic clade of mitotypes, El Hierro is composed of a single monophyletic clade occurring within a larger clade comprising all the La Palma mitotypes, and the mitotypes of these three islands form a monophyletic group distinct from Gran Canaria. New methods for estimating divergence times without the assumption of rate constancy have been used to reconstruct the direction and approximate timing of colonizations among the islands. Colonization has occurred from older to progressionally younger islands, and these colonizations are estimated to have occurred less than 2.6 million years ago, although the timing of the initial colonization of the archipelago is not discernable. New methods for the estimation of diversification rates that use branching times as the analyzed variable have been applied to each island fauna. Hypothesized effects of different levels of recent volcanism among islands were not apparent. All islands exhibit a gradually decreasing rate of genetic diversification that is marked by periodic sudden changes in rate.     

Intraspecific evolution of Canary Island Plecotine bats,based on mtDNA sequences

Island differentiation and relationships with congenerics were investigated in the endemic Canary Island bat Plecotus teneriffae, based on approximately 1 kb of mtDNA from the 16S rRNA and cytochrome b genes. P. teneriffae had closer affinities with P. austriacus than with P. auritus. Levels of differentiation between Canary Islands were quite high relative to Pipistrelle-like bats, consistent with philopatric behaviour in the Plecotus genus. Cladogenesis within P. teneriffae appears to have occurred after the emergence of the islands of El Hierro and La Palma during the Pleistocene. An intraspecific network shows that haplotypes from the younger islands of La Palma and El Hierro are connected to the Tenerife haplotype by a similarly large number of mutational steps. This suggests that they were both colonised at a similar time from the much older island of Tenerife. The other Plecotine bat species, Barbastellus barbastellus shows close affinities with B. barbastellus from mainland Spain, with levels of mtDNA divergence being comparable with intraspecific variation within other mammal species.     

Paraphyly of the Blue Tit (Parus caeruleus) suggested from cytochrome b sequences

The phylogenetic relationships of the Blue Tit-Azure Tit assemblage (genus Parus; Aves: Passeriformes) were studied using mitochondrial DNA sequences of 24 specimens representing seven subspecies from Eurasia and North Africa. Previous work based on comparative morphological and acoustic data suggested a division of the Blue Tit (Parus caeruleus) into two species. Our analyses clearly indicate that the Blue Tit represents a paraphyletic assemblage, including a European/Middle Asian clade that is the sister group to the Azure Tit (Parus cyanus) and a North African clade. The North African clade (teneriffae subspecies group) is a sister group to the European Blue Tit/Azure Tit clade. We suggest a division of the Blue Tit into two separate species, Eurasian Blue Tit (Parus caeruleus s. str.) and African Blue Tit (Parus teneriffae). However, our data give no support for assigning species rank to Parus cyanus flavipectus, a subspecies of the Azure Tit, as suggested by several authors on morphological grounds.     

The evolutionary history of Afrocanarian blue tits inferred from genomewide SNPs

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.     

Molecular evidence for adaptive radiation of Micromeria Benth. (Lamiaceae) on the Canary Islands as inferred from chloroplast and nuclear DNA sequences and ISSR fingerprint data

The Canary Islands have been a focus for phylogeographic studies on the colonization and diversification of endemic angiosperm taxa. Based on phylogeographic patterns, both inter island colonization and adaptive radiation seem to be the driving forces for speciation in most taxa. Here, we investigated the diversification of Micromeria on the Canary Islands and Madeira at the inter- and infraspecific level using inter simple sequence repeat PCR (ISSR), the trnK-Intron and the trnT-trnL-spacer of the cpDNA and a low copy nuclear gene. The genus Micromeria (Lamiaceae, Mentheae) includes 16 species and 13 subspecies in Macaronesia. Most taxa are restricted endemics, or grow in similar ecological conditions on two islands. An exception is M. varia, a widespread species inhabits the lowland scrub on each island of the archipelago and could represent an ancestral taxon from which radiation started on the different islands. Our analyses support a split between the "eastern" islands Fuerteventura, Lanzarote and Gran Canaria and the "western" islands Tenerife, La Palma and El Hierro. The colonization of Madeira started from the western Islands, probably from Tenerife as indicated by the sequence data. We identified two lineages of Micromeria on Gomera but all other islands appear to be colonized by a single lineage, supporting adaptive radiation as the major evolutionary force for the diversification of Micromeria. We also discuss the possible role of gene flow between lineages of different Micromeria species on one island after multiple colonizations.     

Mate choice and imprinting in birds studied by cross-fostering in the wild

Sexual-selection theories generally assume that mating preferences are heritable traits. However, there is substantial evidence that the rearing environment may be important for the development of mating preferences, indicating that they may be learnt, or modified by experience. The relative importance of such sexual imprinting across species remains largely unexplored. Here, we report results of a large-scale cross-fostering experiment in the wild in which nestling birds were raised by parents of a different species. We show that resulting sexual imprinting may have a negative effect on pairing success in one species (the great tit, Parus major), but not in two other species (the blue tit, P. caeruleus and the pied flycatcher, Ficedula hypoleuca). A remarkable variation thus seems to exist, even between species that are congeneric and have similar breeding ecologies. The cross-fostering resulted in heterospecific pairings between the two tit species (female blue tit breeding with male great tit), which has never, to our knowledge, been previously documented. However, the chicks fledging from these nests were all blue tit.     

Integrative taxonomy reveals Europe's rarest songbird species,the Gran Canaria blue chaffinch Fringilla polatzeki

The conservation of endangered taxa often critically depends on accurate taxonomic designations. The status of the Gran Canaria population of the blue chaffinch Fringilla teydea polatzeki has not been reevaluated since the early 1900s when this taxon was described as a subspecies and combined with the much more common Tenerife blue chaffinch F. t. teydea in a single species. We show that multiple diagnostic differences in plumage, songs, calls and morphometrics distinguish F. t. polatzeki from F. t. teydea. Preliminary playback experiments suggest that F. t. polatzeki is able to discriminate between songs of both taxa. Along with previously reported differences in mitochondrial DNA, these findings show that the blue chaffinches on Gran Canaria and Tenerife represent two distinctive species: F. polatzeki and F. teydea. Gran Canaria blue chaffinch is Europe's rarest passerine species and should be classified as critically endangered. Its long‐term survival in the wild currently depends on a very small (< 20 km²) area in southwest Gran Canaria. Reclassification of Gran Canaria blue chaffinch as a species increases the urgency of ongoing conservation efforts. Our study underscores the critical importance of taxonomic clarification of threatened taxa that are currently classified as ‘subspecies’.     

Phylogenetic relationships among the Canary Island Steganacaridae (Acari, Oribatida) inferred from mitochondrial DNA sequence data

The mite genus Steganacarus is represented in the Canary Islands by three endemic species, one recently discovered species, and several morphotypes of uncertain taxonomic position. We used a fragment of the mitochondrial cytochrome oxidase I gene to reconstruct the phylogenetic relationships among representatives of the different taxa from the three central islands of the archipelago, Tenerife, La Gomera and Gran Canaria. Sequence data were analysed by both maximum parsimony and maximum likelihood methods. The inferred phylogenetic relationships do not correlate well with current morphological taxonomy but reveal four deeply divergent and geographically coherent lineages, one each on Gran Canaria and La Gomera and two on Tenerife. No pattern of molecular differentiation was observed among different morphotypes. Possible explanations for this incongruence are suggested in relation to the ecology and biogeography of the group. A recently discovered Steganacarus species from La Gomera, morphologically quite distinct from the other Canarian Steganacarus, is clearly identified as a taxon distantly related to all the other Canarian samples.     

Glacial history and colonization of Europe by the blue tit Parus caeruleus

Mitochondrial control region sequences from European populations of the blue tit Parus caeruleus were used to reveal the Pleistocene history and the post-glacial recolonization of Europe by the species. The southern subspecies, P. c. ogliastrae was found to represent a stable population with isolation-by-distance structure harboring a lot of genetic variation, and the northern subspecies P. c. caeruleus a recently bottlenecked and expanded population. We suggest that after the last Ice Ages, the subspecies have colonized Europe from two different southern refuges following previously proposed general recolonization routes from the Balkans to northern and Central Europe, and from the Iberian Peninsula north- and eastwards. The two subspecies form a wide secondary contact zone extending from southern Spain to southern France.     

Index to Vegetatio,volumes 74–110 (1988–1994)

Chamaecytisus proliferus (L.fil.) Link (Fabaceae: Genisteae) represents a species complex in the Canary Islands. Floristic data from 147 releves from the whole complex were collected and analysed by classification (TWINSPAN) and ordination (DECORANA) methods. Results indicate that white escobon of Tenerife, escobon of El Hierro, white escobon of Gran Canaria and typical tagasaste in La Palma are associated with those plant communities from the north of these islands which are under the influence of the north-eastern trade winds. Narrow-leaved escobon in Tenerife and La Gomera, escobon of southern Gran Canaria and white tagasaste of La Palma are found in those areas which are not under the direct influence of these winds. Morphological forms from the more easterly islands (Gran Canaria and Tenerife-La Gomera) have the broadest ecological range and they have played an important role in the floristic changes which have taken place after the destruction of the forests in these islands. The highest priorities for in situ conservation should be given to wild populations of typical tagasaste, white escobon of Tenerife and escobon of El Hierro.Abbreviations IBPGR International Board for Plant Genetic Resources - DECORANA Detrended Correspondence Analysis - OTU Operational Taxonomic Unit - TWINSPAN Two Way Indicator Species Analysis     

Tracking colonization and diversification of insect lineages on islands: mitochondrial DNA phylogeography of Tarphius canariensis (Coleoptera: Colydiidae) on the Canary Islands.

The genus Tarphius Erichson (Coleoptera: Colydiidae) is represented by 29 species on the Canary Islands. The majority are rare, single-island endemics intimately associated with the monteverde (laurel forest and fayal-brezal). The Tarphius canariensis complex is by far the most abundant and geographically wide-spread, occurring on Gran Canaria, Tenerife and La Palma. Eighty-seven individuals from the T. canariensis complex were sequenced for 444 bp of the mitochondrial DNA cytochrome oxidase I gene (COI), 597 bp of the COII gene and the intervening tRNA(leu) gene. A neighbour-joining analysis of maximum-likelihood distances put La Palma as a single monophyletic clade of haplotypes occurring within a larger clade comprising all Tenerife haplotypes. Gran Canarian haplotypes were also monophyletic occurring on a separate lineage. Using a combination of the phylogeographic pattern for T. canariensis, geological data, biogeography of the remaining species and estimated divergence times, we proposed a Tenerifean origin in the old Teno massif and independent colonizations from here to north-eastern Tenerife (Anaga), Gran Canaria and La Palma. New methods of estimating diversification rates using branching times were applied to each island fauna. All islands exhibited a gradually decreasing rate of genetic diversification similar to that seen for Brachyderes rugatus (Coleoptera: Curculionidae) from the Canary Islands.     

Status and relationships of the extinct giant Canary Island lizard Gallotia goliath (Reptilia: Lacertidae), assessed using ancient mtDNA from its mummified remains

Ancient mitochondrial DNA sequences (378 base pairs of cytochrome b and 368 of 12S rRNA) extracted from a mummified extinct giant lizard, Gallotia goliath , from eastern Tenerife, Canary Islands, were used to assess the species status and relationship of this form within the genus. G. goliath is clearly a member of the G. simonyi group of the western Canary islands (Tenerife, La Gomera, El Hierro and La Palma) and is not closely related to the giant G. stehlini of Gran Canaria. Contrary to recent opinion, it is phylogenetically distinct, within the G. simonyi group, from the extant G. simonyi of El Hierro and also from the recently discovered live G. gomerana on La Gomera and from G. intermedia in north-western Tenerife. It may be the sister taxon of either all the other members of the G. simonyi group or of G. intermedia . The phylogenetic distinctness of G. goliath makes Tenerife unique among oceanic islands in having had one giant and two medium-sized lizard species that were probably substantially herbivorous, the others being G. intermedia and G. galloti . Gallotia shows great community differences on other islands in the Canaries, two having a single small species, one a single giant, and three a giant and a medium-sized form. © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 80 , 659–670.     

Sexual imprinting and the origin of obligate brood parasitism in birds

We discuss two pathways along which obligate brood parasitism (OBP) may evolve and examine some of the critical steps that must be passed by letting great tits Parus major be reared by blue tits Parus caeruleus in a field experiment. The cross-fostered chicks survived well in blue tit nests, but their local recruitment and reproductive success was much lower than that of controls. The effect was strongest when great tits grew up with siblings of the host species rather than with conspecific siblings in blue tit nests. The low success seemed to be caused by misimprinting because the cross-fostered birds behaved like blue tits in several aspects (species association, alarm calls, and aggressive response by resident females to caged intruders). Some birds of both sexes were apparently so strongly imprinted that they did not attract or accept a social mate of their own species. We conclude that imprinting may be necessary for OBP to evolve in birds because the parasite must be attracted to the nests of the host species to add eggs and thereby continue the parasitic life cycle. However, strong imprinting may also prevent OBP from occurring if parasitic offspring seek a mate from the host species.     

A review on the impacts of feral cats (Felis silvestris catus) in the Canary Islands: implications for the conservation of its endangered fauna

Feral cats have been directly responsible for the extinction of numerous species on islands worldwide, including endemic species of mammals, birds and reptiles. The diet of feral cats in the main habitats of the Canary Islands, as generally occurred on oceanic islands, is mainly composed of introduced mammals, and native species of birds, reptiles and insects. The impact of feral cat upon the endangered species was assessed by evaluating their relative abundance in the cats’ diet and by considering their current conservation status. A total of 68 different preys were identified at species level in all studies carried out in the Canary Islands (5 mammals, 16 birds, 15 reptiles and 32 invertebrates). From all the species preyed by feral cats in the Canary Islands, only four of them are considered threatened by the IUCN Red List of Threatened Species: one endemic bird Saxicola dacotiae and three endemic giant lizards, Gallotia simonyi, Gallotia intermedia, and Gallotia gomerana. Although some efforts on management control have been carried out, it is necessary to enforce these conservation activities on those areas of Tenerife, La Gomera and El Hierro where giant lizards are still present. Furthermore some local areas where endangered bird species are highly predated should be protected. Nevertheless, it is important to take into account the presence of other introduced species such as rats, mice or rabbits in order to avoid problems derived from the hyperpredation process and mesopredator release effect.     

Evolution and genetic structure of the great tit (Parus major) complex

The great tit complex is divided into four groups, each containing several subspecies. Even though the groups are known to differ markedly on morphological, vocal and behavioural characters, some hybridization occurs in the regions where they meet. The great tit has often been referred to as an example of a ring species, although this has later been questioned. Here, we have studied the genetic structure and phylogenetic relationships of the subspecies groups to clarify the evolutionary history of the complex using control region sequences of the mitochondrial DNA. The subspecies groups were found to be monophyletic and clearly distinct in mitochondrial haplotypes, and therefore must have had long-independent evolutionary histories. This conflicts with the ring species assignment and supports the formation of secondary contact zones of previously temporarily isolated groups. According to the phylogenetic species concept, all the subspecies groups could be considered as separate species, but if the definition of the biological species concept is followed, none of the subspecies groups is a true species because hybridization still occurs.     

Microsatellite loci isolation in the endangered Gran Canarian blue chaffinch (Fringilla teydea polatzeki) and their utility in closely related taxa

The blue chaffinch, Fringilla teydea, is an endemic species of the Canary Islands. This species is formed by two subspecies: The Teneriffean blue chaffinch (F. t. teydea), and the endangered Gran Canarian blue chaffinch, (F. t. polatzeki). Here we report the isolation and characterization of nine tetranucleotide microsatellites (AAAG and AAAT) from the Gran Canarian subspecies, using an enrichment protocol. An average of 7.8 alleles per locus and an average observed heterozygosity of 0.773 were found (n = 28). The loci were tested for their ability to cross amplify in the Teneriffean subspecies and in the common chaffinch (Fringilla coelebs). These microsatellites will be used to manage a captive breeding programme for the endangered Gran Canarian subspecies.     

Characterization of MHC-I in the blue tit (Cyanistes caeruleus) reveals low levels of genetic diversity and trans-population evolution across European populations

The major histcompatibility complex (MHC) is a vital component of the adaptive immune system in all vertebrates. This study is the first to characterize MHC class I (MHC-I) in blue tits (Cyanistes caeruleus), and we use MHC-I exon 3 sequence data from individuals originating from three locations across Europe: Spain, the Netherlands to Sweden. Our phylogeny of the 17 blue tit MHC-I alleles contains one allele cluster with low nucleotide diversity compared to the remaining more diverse alleles. We found a significant evidence for balancing selection in the peptide-binding region in the diverse allele group only. No separation according to geographic location was found in the phylogeny of alleles. Although the number of MHC-I loci of the blue tit is comparable to that of other passerine species, the nucleotide diversity of MHC-I appears to be much lower than that of other passerine species, including the closely related great tit (Parus major) and the severely inbred Seychelles warbler (Acrocephalus sechellensis). We believe that this initial MHC-I characterization in blue tits provides an important step towards understanding the mechanisms shaping MHC-I diversity in natural populations.     

Evolution and diversification of the forest and hypogean ground-beetle genus Trechus in the Canary Islands

The beetle genus Trechus (Carabidae) is represented in the Macaronesian Islands by 43 endemic species. The Canary Islands have 16 endemic species, with two adapted to hypogean life. Phylogenetic relationships among 177 individuals of 38 Canarian, Madeiran, Azorean and continental Trechus species were examined using mitochondrial DNA and nuclear internal transcribed spacer 2 (ITS2) sequence data. Results show two main lineages in the Canaries: one comprising two sister groups with species from the laurel forest of La Gomera and Tenerife, and the other containing the single species from Gran Canaria and a species complex in the four western islands including two troglobites. Calibrations were applied to a linearized tree using a relaxed molecular clock method to estimate the major evolutionary divergence times of the Canarian Trechus species. Although the species assemblage in this archipelago is relatively ancient (7-8 million years), much of the species diversity is recent. Transition to the hypogean environment is more consistent with the "adaptive shift" rather than with the competing "climatic relict" hypothesis.