The evolution of the Indian Ocean parrots (Psittaciformes): Extinction, adaptive radiation and eustacy

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Abstract

Parrots are among the most recognisable and widely distributed of all bird groups occupying major parts of the tropics. The evolution of the genera that are found in and around the Indian Ocean region is particularly interesting as they show a high degree of heterogeneity in distribution and levels of speciation. Here we present a molecular phylogenetic analysis of Indian Ocean parrots, identifying the possible geological and geographical factors that influenced their evolution. We hypothesise that the Indian Ocean islands acted as stepping stones in the radiation of the Old-World parrots, and that sea-level changes may have been an important determinant of current distributions and differences in speciation. A multi-locus phylogeny showing the evolutionary relationships among genera highlights the interesting position of the monotypic Psittrichas, which shares a common ancestor with the geographically distant Coracopsis. An extensive species-level molecular phylogeny indicates a complex pattern of radiation including evidence for colonisation of Africa, Asia and the Indian Ocean islands from Australasia via multiple routes, and of island populations ‘seeding’ continents. Moreover, comparison of estimated divergence dates and sea-level changes points to the latter as a factor in parrot speciation. This is the first study to include the extinct parrot taxa, Mascarinus mascarinus and Psittacula wardi which, respectively, appear closely related to Coracopsis nigra and Psittacula eupatria.

Highlights

► Adaptive radiation of Old-World parrots. ► Indian Ocean islands “seeded” continental Africa and Asia. ► Changes in sea-level influenced the pattern of adaptive radiation. ► Extinct Mascarene parrot resolved as a Coracopsis genus parrot rather than Psittacula. ► Extinct Seychelles parakeet resolved as an Alexandrine parrot.

Introduction

The Indian Ocean islands are remarkable for their high levels of biodiversity and endemism, and the region has become an important focus for evolutionary research. This high biodiversity is explained by the ecological diversity and the complex geological history (Hall, 1996, Hall, 1997) of the region. In particular, the Indian Ocean islands have diverse avifauna, and available fossil data and historical documentation suggests that they may have been especially rich in parrot species; virtually all Indian Ocean island systems currently support or have supported parrot taxa (Hume, 2007). The surrounding continents also have many parrot species, suggesting that the islands may have been important stepping stones in the adaptive radiation of these birds.

In an extensive review of anatomical, morphological and behavioural evidence, Smith (1975) suggested a single parrot family subdivided into four subfamilies – the Platycercinae (with four tribes), Loriinae (with five tribes), Arinae and Psittacinae. Forshaw (1989) largely accepted Smith’s tribal arrangements but redistributed them among three subfamilies, the Loriinae (no tribes), Cacatuinae (three tribes) and Psittacinae (nine tribes). Recent reviews (Collar, 1997, Forshaw, 2006) split the parrots into two families, Cacatuidae (cockatoos) and Psittacidae (‘true parrots’), the latter of which is itself divided into Loriinae (lorikeets), Psittacinae (parrots and macaws), Strigopinae (New Zealand parrots), Psittrichadinae (the vulturine parrot) and Micropsittinae (the pygmy parrots) subfamilies. Further studies indicated that the Strigopinae parrots actually form a third family, Strigopidae (de Kloet and de Kloet, 2005, Wright et al., 2008). Analyses have also cast doubt on Forshaw’s placement of Psittrichas fulgidas as the sole member of Psittrichadinae. Whilst these molecular phylogenetic analyses have not unambiguously identified the evolutionary position of Psittrichas, they do suggest a close relationship with Coracopsis, a genus belonging to Psittacinae (de Kloet and de Kloet, 2005, Schweizer et al., 2009, Wright et al., 2008). Forshaw (2006) split Psittacinae into six tribes: Psittacini (Afrotropical parrots), Psittaculini (psittaculine parrots), Arini (Neotropical parrots), Cyclopsittacini (fig parrots), Polytelini and Platycercini (broad-tailed parrots). Most of the parrots distributed in Africa and Asia, including those found on Indian Ocean islands and some from Australia, have been referred to Psittacini and Psittaculini. Psittacini includes Coracopsis, Poicephalus and Psittacus; Psittaculini, which is found in Australasia, Africa and Asia, comprises Agapornis, Alisterus, Aprosmictus, Eclectus, Geoffroyus, Loriculus, Polytelis, Prioniturus, Psittacella, Psittacula, Psittinus and Tanygnathus.

The parrots occurring in the Indian Ocean region show considerable range and population heterogeneity. Some genera are highly speciose and widely dispersed across islands and continents (Groombridge et al., 2004), whilst others show strong geographical restriction (Fig. 1) and little morphological diversification (Forshaw, 2006, Juniper and Parr, 1998). These striking contrasts make the parrots of this region an excellent system in which to answer questions about the biogeographic factors that influence speciation and adaptation. Numerous studies have attempted to resolve parrot systematics using both morphological and molecular techniques (Astuti et al., 2006, Birt et al., 1992, de Kloet and de Kloet, 2005, Hume, 2007, Mayr, 2010, Sibley and Ahlquist, 1990, Wright et al., 2008). Most recent molecular phylogenetic studies (Astuti et al., 2006, de Kloet and de Kloet, 2005, Schweizer et al., 2009, Wright et al., 2008) have encompassed parrot genera from across the clade’s distribution giving a perspective of the broad evolutionary trends. However, sampling from within each genus has been comparatively restricted, particularly for Coracopsis and Psittacula which are important in the context of parrot evolution in the Indian Ocean. Here we seek to understand the species and subspecies relationships that underpin the adaptive radiation of Old-World parrots in and around the Indian Ocean islands. Specifically, by comparing the evolutionary history of island parrots (Coracopsis, Eclectus and Tanygnathus) with that of continental taxa (Agapornis, Aprosmictus, Poicephalus, Polytelis and Psittacus) and with those distributed both continentally and on islands (Loriculus and Psittacula), we aim to identify the biogeographical factors that influenced the adaptive radiation of parrots. This selected group of taxa also encompasses a range of species richness – Aprosmictus, Eclectus, Psittacus and Tanygnathus are monotypic, Psittacula is highly speciose; Agapornis, Coracopsis, Loriculus, Poicephalus and Polytelis show intermediate levels of diversity. Initially, we seek to confirm the genus-level relationships identified by previous studies (Schweizer et al., 2009, Wright et al., 2008) through a multi-locus phylogeny of genera in this region: Agapornis, Aprosmictus, Coracopsis, Eclectus, Loriculus, Poicephalus, Polytelis, Psittacula and Psittacus. We then establish species-level relationships to understand the radiation of these genera and the role of Indian Ocean islands. We substantially increase the sampling of parrot species and subspecies over that in previous studies. In particular, we include most of the known Psittacula and Coracopsis taxa, and provide increased taxon coverage for Agapornis, Poicephalus and Loriculus. We also attempted to resolve the phylogenetic relationships of the extinct Psittacula wardi, Mascarinus mascarinus, Psittacula exsul and Psittacula eques. These are iconic examples of island-endemics that were found in the Mascarenes or Seychelles. They are known only from a small number of preserved skins (Hume, 2007) and early accounts (Cheke and Hume, 2008), and their origins have confounded evolutionary biologists.

Section snippets

Sampling

The sampling effort was focused upon Coracopsis, Loriculus and Psittacula. These genera are distributed in and around the islands of the Indian Ocean and are thus most informative to understanding the adaptive radiation of parrots in this region. Additionally Coracopsis and Psittacula have not been well-sampled in previous studies: Coracopsis has been limited to Coracopsis vasa vasa and Coracopsis nigra nigra, and Psittacula to Psiitacula columboides and/or Psittacula eupatria (Schweizer et

Results

All sequences produced by this study have been submitted to GenBank, accession numbers GQ996495GQ996517 (Table 1). Of the extinct parrots sequence data were successfully obtained from P. wardi (708 bp) and M. mascarinus (740 bp), but not from P. exsul and P. eques (there was insufficient tissue to repeat the extractions using alternative techniques).

Bayesian and maximum likelihood phylogenetic analyses using the multi-locus data recovered the same tree topology. The genus-level relationships

Discussion

In common with previous studies (Schweizer et al., 2009, Wright et al., 2008) the phylogenetic analyses presented here indicate a complex pattern of evolution in the Old-World parrots involving transoceanic dispersal and multiple adaptive radiation events mediated by the islands in the Indian Ocean. The results also help to resolve the phylogenetic position of two important extinct parrot taxa. The affinity of the extinct P. wardi with P. eupatria has long been suggested (Jones, 1987, Penny,

Concluding remarks

The Indian Ocean has become an important focus of phylogeographical research not least because of the apparent influence of geological dynamism and geographical complexity on the evolution of the region’s biota. This study highlights the complex pattern of evolution in the parrots that occur in this region and the apparent role of geological events such as eustacy and plate tectonics. However, a degree of caution is required in the interpretation of molecular dates in the context of geological

Acknowledgments

The authors thank Julian Pender Hume, Michael Brooke, Ross McEwing, Anne Previato, Eric Pasquet, Bob McGowan, Roger Safford, Paul Michael-Agapow and Anthony Cheke. This work was supported by a research grant from the Systematics Research Fund to Jim Groombridge and a grant from the Natural History Museum’s Zoology Research Fund to Robert Prys-Jones.

References (43)

  • A.J. Drummond et al.

    BEAST: Bayesian evolutionary analysis by sampling trees

    BMC Evolutionary Biology

    (2007)
  • J.M. Forshaw

    Parrots of the World

    (1989)
  • J.M. Forshaw

    Parrots of the World

    (2006)
  • S. Guindon et al.

    A simple, fast and accurate algorithm to estimate large phylogenies by maximum likelihood

    Systematic Biology

    (2003)
  • M. Hachisuka

    The Dodo and Kindred Birds, or the Extinct Birds of the Mascarene Islands

    (1953)
  • R. Hall

    Reconstructing Cenozoic SE Asia

  • R. Hall

    Cenozoic plate tectonic reconstructions of SE Asia

  • B.U. Haq et al.

    Chronology of fluctuating sea levels since the Triassic

    Science

    (1987)
  • S.B. Hedges et al.

    Continental breakup and the ordinal divergence of birds and mammals

    Nature

    (1996)
  • K. Helm-Bychowski et al.

    Recovering phylogenetic signal from DNA sequences, relationships within the corvine assemblage (class Aves) as inferred from complete sequences of the mitochondrial DNA cytochrome b gene

    Molecular Biology and Evolution

    (1993)
  • J.P. Hume

    Reappraisal of the parrots (Aves: Psittacidae) from the Mascarene Islands, with comments on their ecology, morphology, and affinities

    Zootaxa

    (2007)
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