Age, origins and extinctions of the avifauna of Macaronesia: a synthesis of phylogenetic and fossil information
Graphical abstract
Highlights
► Molecular and paleontological data key to understand evolution in oceanic islands. ► Extant birds colonized macaronesian archipelagos within the last four million years. ► Fossil records support the idea that higher species richness previously existed. ► Extinction data suggests an extinction process mediated by man.
Introduction
Investigating the origin and diversification of oceanic island biotas has been a key focus of biogeography, evolutionary biology and conservation biology (MacArthur and Wilson, 1967, Emerson and Kolm, 2005, Filardi and Moyle, 2005, Savolainen et al., 2006, Steadman, 2006, Grant and Grant, 2008, Ricklefs, 2010a). During the last two decades, the use of molecular markers has provided new insights into the evolutionary histories of a great many taxa, and the resulting conclusions have often challenged biogeographic and evolutionary ideas based on classical taxonomy (e.g. Raxworthy et al., 2002, Jordal et al., 2004, Glor et al., 2005, Macias-Hernandez et al., 2008). Phylogeographic syntheses may provide a framework for a general understanding of colonization and diversification within the biotas of archipelagos with different physical and ecological conditions such as age, latitude, altitude and distance to mainland (Ricklefs, 2010a, Ricklefs, 2010b). The reconstruction of ancestral distributions and hypotheses about the diversification of taxa have typically used data from extant species, as comprehensive paleontological information on a regional scale is often unavailable. However such analyses may result in biased interpretations if now extinct species are a non-random subset of species, and/or are informative with regard to complex ecological interactions and diversification within a community. Multidisciplinary approaches incorporating information from geology, archaeology, palaeontology and genetics could minimize these limitations and potential biases (Crisci et al., 2003).
Recently, taxa of the North Atlantic Macaronesian islands have become a focus for molecular studies of colonization and diversification of oceanic biotas. Many of these studies have focused on groups of organisms with high rates of diversification such as plants, invertebrates and reptiles (Juan et al., 2000, Emerson, 2002, Emerson, 2003, Kim et al., 2008). Macaronesian birds exhibit a significant number of endemic species and subspecies (Stattersfield et al., 1998, Martín and Lorenzo, 2001), but have only more recently become the subject of phylogeographic study. These studies have revealed diverse evolutionary histories within species, or species complexes, including strong genetic differentiation between islands (Pestano et al., 2000, Dietzen et al., 2003, Kvist et al., 2005, Päckert et al., 2006), incipient differentiation and contemporary gene flow (Hille et al., 2003, Illera et al., 2007, Barrientos et al., 2008, Spurgin et al., 2011) and reverse colonization (Illera et al., 2011). However, the extent to which the overall macaronesian avifauna is the result of ancient or recent colonization and diversification events has not yet been addressed. In light of recent phylogenetic analyses of macaronesian terrestrial taxa such as insects and plants, we may expect to find both old and young evolutionary lineages (e.g. Emerson, 2008, Aigoin et al., 2009). Even though the avian radiation in the region is less spectacular than in other archipelagos such as those of the Pacific and Indian Oceans that does not necessarily mean that extant lineages are themselves young. In addition to molecular phylogenetic and phylogeographic data, fossil data may provide complementary insight into the evolutionary history and community composition of the avifauna of a region. Recent radiocarbon dating on bone collagen of extinct taxa is generating more rigorous approximations of species extinction dates and thus allowing us to better infer the causes of such extinctions. Fossil data can also contribute to a broader understanding of historical faunas and community composition, providing indirect inferences about past environments and ecological interactions.
The aim of this review is to develop a general understanding of the evolutionary and biogeographic history of the macaronesian avifauna by synthesising information from phylogenetic, phylogeographic and paleontological studies that yield information on colonization, diversification and extinction within this group. We then compare patterns for Macaronesia with those of other oceanic archipelagos to evaluate to what extent patterns may be generalised across regions, but also to identify knowledge gaps that should be the focus of future research.
Section snippets
Macaronesia
The macaronesian region consists at 31 principal volcanic islands in the north eastern Atlantic Ocean with floral and faunal affinities to the African and European mainland (Juan et al., 2000, Gillespie and Clague, 2009). The islands are grouped into five archipelagos (Azores, Madeira, Selvagens, Canary Islands and Cape Verde) situated between 39°N 31°W and 15°N 23°W (Fig. 1). The broad range of distances between archipelagos and the mainland (<100 km for the Canary Islands and 1365 km for
Geographic origins
The taxonomic affinities of native bird species suggest that the origin of the extant terrestrial macaronesian avifauna is largely from the closest Palaearctic mainland areas, although the Cape Verde archipelago, due to its much lower latitude and proximity to Africa, contains species related to the semi-arid African mainland region (Hazevoet, 1995, Martín and Lorenzo, 2001, Clarke et al., 2006). Recent phylogenetic analyses have confirmed the close relationships between endemic macaronesian
Patterns and processes
Recent paleontological studies in Madeira and the Canary Islands are now changing perceptions about the diversification, distribution, and composition of terrestrial avian communities on these islands (S-Table 3). Upper Pleistocene-Holocene fossil records reveal endemic species extinctions among bird families such as Procellariidae (shearwaters), Phasianidae (quails), Rallidae (rails), Strigidae (owls), Turdidae (thrushes) and Fringillidae (finches and buntings) (Pieper, 1985, Alcover and
Conclusions
This review indicates that, despite the relatively old (Miocene: ca 5–29 my) age of the majority of the macaronesian islands, the extant avian lineages on these islands appear to have colonized the region relatively recently (less than four my). Fossil records suggest that greater species richness existed in the past, and that the arrival of aboriginal people from North Africa (≈2500 yrs), and then the later colonisation of the islands by Europeans both caused significant extinctions.
Acknowledgements
J.C. Illera was funded by a Spanish postdoctoral fellowship (Ramón y Cajal). Mario Díaz and two anonymous reviewers provided valuable comments.
References (137)
- et al.
A reappraisal of the stratigraphy of Cueva del Llano (Fuerteventura) and the chronology of the House Mouse (Mus musculus) introduction into the Canary Islands
Palaeogeogr. Palaeoclim. Palaeoecol.
(2009) - et al.
The volcanotectonic evolution of Flores Island, Azores (Portugal)
J. Volc. Geol. Res.
(2006) - et al.
Radiation, multiple dispersal and parallelism in the skinks, Chalcides and Sphenops (Squamata: Scincidae), with comments on Scincus and Scincopus and the age of the Sahara Desert
Mol. Phyl. Evol.
(2008) - et al.
Relationships and evolution of the North African geckos, Geckonia and Tarentola (Reptilia: Gekkonidae), based on mitochondrial and nuclear DNA sequences
Mol. Phyl. Evol.
(2002) - et al.
Evolution and diversification of the forest and hypogean ground-beetle genus Trechus in the Canary Islands
Mol. Phyl. Evol.
(2007) - et al.
Divergence times and colonization of the Canary Islands by Gallotia lizards
Mol. Phyl. Evol.
(2010) - et al.
Faunal histories from Holocene ancient DNA
TREE
(2011) - et al.
Biogeography origin and radiation of the Old World crocidurine shrews (Mammalia: Soricidae) inferred from mitochondrial and nuclear genes
Mol. Phyl. Evol.
(2008) - et al.
A volcanological and geochemical investigation of Boa Vista, Cape Verde Islands; 40Ar/39Ar geochronology and field constraints
J. Volc. Geol. Res.
(2010) - et al.
Earlier history of the ≥70-Ma-old Canary hotspot based on the temporal and geochemical evolution of the Selvagen Archipelago and neighboring seamounts in the eastern North Atlantic
J. Volc. Geo. Res.
(2001)
Assessing ancient DNA studies
TREE
Phylogeography of the Calonectris shearwaters using molecular and morphometric data
Mol. Phyl. Evol.
A molecular phylogeny of African kestrels with reference to divergence across the Indian Ocean
Mol. Phyl. Evol.
Phylogenetic relationships, biogeography and speciation in the avian genus Saxicola
Mol. Phyl. Evol.
Phylogeny of a Macaronesian radiation: host-plant use and possible cryptic speciation in Liparthrum bark beetles
Mol. Phyl. Evol.
Colonization and diversification: towards a phylogeographic synthesis for the Canary Islands
TREE
Mitochondrial phylogeography of the long-eared bats (Plecotus) in the Mediterranean Palaearctic and Atlantic Islands
Mol. Phyl. Evol.
Colonisation and diversification of the blue tits (Parus caeruleus teneriffae-group) in the Canary Islands
Mol. Phyl. Evol.
Isotopic variations with distance and time in the volcanic islands of the Cameroon line: evidence for a mantle plume origin
Earth Planet. Sci. Lett.
Colonization history of Atlantic island common chaffinches (Fringilla coelebs) revealed by mitochondrial DNA
Mol. Phyl. Evol.
The Lanius excubitor (Aves, Passeriformes) conundrum - taxonomic dilemma when molecular and non-molecular data tell different stories
Mol. Phyl. Evol.
And if Engler was not completely wrong? Evidence for multiple evolutionary origins in the moss flora of Macaronesia
Evolution
Una nueva especie de Carduelis (Fringillidae) de La Palma
Vieraea
Lista preliminar de especies silvestres de Cabo Verde (hongos, plantas y animales terrestres)
Rapid radiation of canaries (Genus Serinus)
Mol. Biol. Evol.
Colonization patterns and genetic structure of peripherals populations of the trumpeter finch (Bucanetes githagineus) from Northwest Africa, the Canary Islands and the Iberian Peninsula
J. Biogr.
Anomalagrion hastatum (Say), an American damselfly indigenous to the Azores (Odonata, Coenagrionidae)
Tijdschr. Entomol.
Avian extinction and mammalian introductions on oceanic islands
Science
Historical contingency and the evolution of a key innovation in an experimental population of Escherichia coli
Proc. Natl. Acad. Sci. U.S.A.
Ein prähistorischer brutplatz von seevögeln auf er insel Sal (Kapverden)
J. Ornithol.
A List of the Terrestrial Fungi, Flora and Fauna of Madeira and Selvagens Archipelagos
A List of the Terrestrial and Marine Biota from the Azores
Extinction patterns in the avifauna of the Hawaiian Islands
Divers. Distribut.
Habitat loss and extinction in the hotspots of biodiversity
Conserv. Biol.
Strong mitochondrial DNA support for a Cretaceous origin of modern avian lineages
BMC Biol.
Ancient DNA provides new insights into the evolutionary history of New Zealand’s extinct Giant Eagle
PLoS Biol.
Is speciation driven by species diversity?
Nature
Canary Islands. Classic Geology in Europe Series
Goats, birds and emergent diseases: apparent and hidden effects of an exotic species in an island environment
Ecol. Appl.
A Field Guide to the Birds of the Atlantic Islands: Canary Islands, Madeira, Azores, Cape Verde
Parthenogenetic Ischnura hastata (Say, 1839), widespread in the Azores (Zygoptera: Coenagrionidae)
Odonatologica
Ages of the Galápagos islands
Avian evolution, Gondwana biogeography and the Cretaceous–Tertiary mass extinction event
Proc. R. Soc. Lond. B
Estudio Geoarqueológico del yacimiento de El Bebedero (Siglos I a.C. a XIV d.C., Lanzarote, Islas Canarias)
Rev. Cuater. Geomorphol.
Historical Biogeography: An Introduction
The long-term ecology of the forest of La Laguna, Tenerife (Canary Islands)
J. Biogr.
Morphometric variability in continental and Atlantic island populations of Chaffinches (Fringilla coelebs)
Evolution
Phylogenetic differentiation of Sylvia species (Aves: Passeriformes) of the Atlantic islands (Macaronesia) based on mitochondrial DNA sequence data and morphometrics
Biol. J. Linn. Soc.
The phylogeographic differentiation of the European robin, Erithacus rubecula, on the Canary Islands revealed by mitochondrial DNA sequence data and morphometrics: evidence for a new robin taxon on Gran Canaria?
Avian Sci.
Phylogeography of island canary (Serinus canaria) populations
J. Ornithol.
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