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Abstract

The Indo-Pacific region has arguably been the most important area for the formulation of theories about biogeography and speciation, but modern studies of the tempo, mode and magnitude of diversification across this region are scarce. We study the biogeographic history and characterize levels of diversification in the wide-ranging passerine bird Erythropitta erythrogaster using molecular, phylogeographic and population genetics methods, as well as morphometric and plumage analyses. Our results suggest that E. erythrogaster colonized the Indo-Pacific during the Pleistocene in an eastward direction following a stepping stone pathway, and that sea-level fluctuations during the Pleistocene may have promoted gene flow only locally. A molecular species delimitation test suggests that several allopatric island populations of E. erythrogaster may be regarded as species. Most of these putative new species are further characterized by diagnostic differences in plumage. Our study reconfirms the E. erythrogaster complex as a 'great speciator': it represents a complex of up to 17 allopatrically distributed, reciprocally monophyletic and/or morphologically diagnosable species that originated during the Pleistocene. Our results support the view that observed latitudinal gradients of genetic divergence among avian sister species may have been affected by incomplete knowledge of taxonomic limits in tropical bird species.
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Research
Cite this article: Irestedt M, Fabre P-H,
Batalha-Filho H, Jønsson KA, Roselaar CS,
Sangster G, Ericson PGP. 2013 The spatio-
temporal colonization and diversification across
the Indo-Pacific by a ‘great speciator’ (Aves,
Erythropitta erythrogaster). Proc R Soc B 280:
20130309.
http://dx.doi.org/10.1098/rspb.2013.0309
Received: 12 February 2013
Accepted: 8 March 2013
Subject Areas:
evolution, taxonomy and systematics, ecology
Keywords:
island biogeography, integrative taxonomy,
speciation, phylogeny, Pleistocene climate
changes
Author for correspondence:
Martin Irestedt
e-mail: martin.irestedt@nrm.se
Electronic supplementary material is available
at http://dx.doi.org/10.1098/rspb.2013.0309 or
via http://rspb.royalsocietypublishing.org.
The spatio-temporal colonization and
diversification across the Indo-Pacific by
a ‘great speciator’ (Aves, Erythropitta
erythrogaster)
Martin Irestedt1, Pierre-Henri Fabre3, Henrique Batalha-Filho4, Knud
A. Jønsson3,5, Cees S. Roselaar6, George Sangster2,7 and Per G. P. Ericson2
1
Department of Biodiversity Informatics and Genetics, and
2
Department of Vertebrate Zoology, Swedish
Museum of Natural History, PO Box 50007, 10405 Stockholm, Sweden
3
Center for Macroecology, Evolution and Climate at the Natural History Museum of Denmark,
University of Copenhagen, Copenhagen, Denmark
4
Departamento de Gene
´tica e Biologia Evolutiva, Instituto de Biocie
ˆncias, Universidade de Sa
˜o Paulo,
Sa
˜o Paulo, Brazil
5
Department of Life Sciences, Imperial College London, Silwood Park campus, Ascot SL5 7PY, UK
6
Naturalis Biodiversity Center, Darwinweg 2, PO Box 9517, 2300 RA Leiden, The Netherlands
7
Department of Zoology, Stockholm University, 10691 Stockholm, Sweden
The Indo-Pacific region has arguably been the most important area for the for-
mulationof theories about biogeography and speciation, but modern studies of
the tempo, mode and magnitude of diversification across this region are scarce.
We study the biogeographic history and characterize levels of diversificationin
the wide-ranging passerine bird Erythropitta erythrogaster using molecular, phy-
logeographic and population genetics methods, as well as morphometric and
plumage analyses. Our results suggest that E. erythrogaster colonized the
Indo-Pacific during the Pleistocene in an eastward direction following a step-
ping stone pathway, and that sea-level fluctuations during the Pleistocene
may have promoted gene flow only locally. A molecular species delimitation
test suggests that several allopatric island populations of E. erythrogaster may
be regarded as species. Most of these putative new species are further charac-
terized by diagnostic differences in plumage. Our study reconfirms the
E. erythrogaster complex as a ‘great speciator’: it represents a complex of up to
17 allopatrically distributed, reciprocally monophyletic and/or morphologi-
cally diagnosable species that originated during the Pleistocene. Our results
support the view that observed latitudinal gradients of genetic divergence
among avian sister species may have been affected by incomplete knowledge
of taxonomic limits in tropical bird species.
1. Introduction
The Indo-Pacific archipelagos have played a fundamental role in the formu-
lation of modern biogeographic and speciation theories. Observations of
the complex distributions of Asian and Australian faunas in the centre of the
region (present-day Wallacea) inspired Alfred Russell Wallace to develop his
ideas on the connection between geography and animal distributions [1,2].
Further east in Melanesia, patterns of geographical variation in birds formed
the basis of Ernst Mayr’s highly influential allopatric model of speciation [3].
A dynamic geological history [4] and Pleistocene sea-level fluctuations [5]
have generated complex patterns of spatio-temporal vicariance events and
dispersal routes [6]. Today, the Indo-Pacific archipelagos comprise more than
20 000 islands ranging from small atolls to large, geologically complex, tropical
islands, such as New Guinea, Sulawesi and Borneo. Several biodiversity hot-
spots have been recognized within the Indo-Pacific region [7], and the largest
island (New Guinea) is estimated to host the third-largest ‘high biodiversity’
wilderness in the world, only surpassed by the Amazon and Congo forests [8].
&2013 The Author(s) Published by the Royal Society. All rights reserved.
... This dynamic makes great speciators an alluring model for investigating how lineage expansion and diversification shape global biodiversity patterns Moyle et al., 2009;Pepke et al., 2019). Molecular phylogenetic studies (Andersen et al., 2013(Andersen et al., , 2014(Andersen et al., , 2015Irestedt et al., 2013;Jønsson et al., 2014;Moyle et al., 2009;Kearns et al., 2020;Pedersen et al., 2018) have confirmed that great speciators represent rapid and geographically complex lineage radiations. However, those same attributes, combined with limited genetic sampling, have impeded precise evolutionary reconstruction of these radiations (though see Gwee et al. [2020] and Manthey et al. [2020]). ...
... We found a significant positive relationship between geographic distance and genetic distance (Supplementary Figure S12; r 2 = 0.47, p <. 001), indicating isolation by distance (Slatkin, 1987(Slatkin, , 1993 and supporting a stepping stone mode of colonization (Cibois et al., 2011;Irestedt et al., 2013). ...
... Diversification of the island thrush occurred during the second half of the Pleistocene, starting c. 1.3 Mya (Supplementary Figure S6). This is in line with dating estimates for other great speciators, which also radiated explosively during the Pleistocene (Andersen et al., 2013(Andersen et al., , 2014(Andersen et al., , 2015Irestedt et al., 2013;Jønsson et al., 2014;Kearns et al., 2020;Moyle et al., 2009;Pedersen et al., 2018). The sequential branching pattern of the island thrush tree (Figure 1) suggests that it expanded across most of its range following a stepping stone colonization path. ...
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Tropical islands are renowned as natural laboratories for evolutionary study. Lineage radiations across tropical archipelagos are ideal systems for investigating how colonization, speciation, and extinction processes shape biodiversity patterns. The expansion of the island thrush across the Indo-Pacific represents one of the largest yet most perplexing island radiations of any songbird species. The island thrush exhibits a complex mosaic of pronounced plumage variation across its range and is arguably the world's most polytypic bird. It is a sedentary species largely restricted to mountain forests, yet it has colonized a vast island region spanning a quarter of the globe. We conducted a comprehensive sampling of island thrush populations and obtained genome-wide SNP data, which we used to reconstruct its phylogeny, population structure, gene flow, and demographic history. The island thrush evolved from migratory Palearctic ancestors and radiated explosively across the Indo-Pacific during the Pleistocene, with numerous instances of gene flow between populations. Its bewildering plumage variation masks a biogeographically intuitive stepping stone colonization path from the Philippines through the Greater Sundas, Wallacea, and New Guinea to Polynesia. The island thrush's success in colonizing Indo-Pacific mountains can be understood in light of its ancestral mobility and adaptation to cool climates; however, shifts in elevational range, degree of plumage variation and apparent dispersal rates in the eastern part of its range raise further intriguing questions about its biology.
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... In fact, most evolutionary radiations on islands are less spectacular from a species-richness, morphological, and niche-differentiation perspective than those famous radiations. Insular radiations tend to be the result of geographic isolation with a strong effect of genetic drift, sexual selection, introgression, and mutation-order speciation (Losos and Ricklefs 2009;Nosil and Flaxman 2011;Warren et al. 2012;Irestedt et al. 2013;Gwee et al. 2020;Recuerda et al. 2021). ...
... Genomics now allows us to reconstruct evolutionary relationships with increased confidence (Lee & Palci, 2015), although it is still challenging for those clades that radiate rapidly, such as many great speciators (Moyle et al., 2009). The condensed sequence of cladogenetic events and increased levels of incomplete lineage sorting (ILS) driven by rapid radiation (DeRaad et al., 2023) and recent divergence (Irestedt et al., 2013) complicate phylogenetic inference (Meleshko et al., 2021). Additionally, gene flow can lead to reticulate evolution (Xu, 2000). ...
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Geographic isolation plays a pivotal role in speciation by restricting gene flow between populations through distance or physical barriers. However, the speciation process is complex, influenced by the interplay between dispersal ability and geographic isolation, especially in "great speciators" - bird species present on multiple islands that, at the same time, have many subspecies. Comparing population differentiation in both continental and insular settings can help us to understand the importance of geographical context in the emergence of great specia-tors. The highly diverse white-eye family Zosteropidae includes several great speciators, including the silvereye (Zosterops lateralis) which consists of 16 subspecies, 11 occurring on islands. The distribution of the silvereye on the Australian continent and numerous southwest Pacific islands allows us to explore the influence of different forms of geographic isolation on population divergence. To do this, we conducted a comprehensive phyloge-nomic analysis of the silvereye and compared patterns of population divergence in insular versus continental silvereye populations. We estimate that the silvereye lineage emerged approximately 1.5 million years ago, followed by the split of the two main silvereye clades: Southern Melanesia and the broader South Pacific (encompassing Australia, New Zealand, and outlying islands). Continental populations show low genetic population structure, which suggests that they can overcome multiple forms of geographic barriers across long distances. In contrast, most island populations are highly structured even over relatively short distances. Divergence statistics further support the idea that water barriers lead to a higher population differentiation when compared to continental distances. Our results indicate that islands promote divergence and provide an empirical example of the geographical conditions that result in the emergence of great speciators.
... Because patterns of morphological, bioacoustic, and genetic diversification are not necessarily spatially congruent in avian taxa, a sound species diagnosis should rely on a combination of all these three sets of diagnostic markers in an integrative approach (Padial et al. 2010;Sangster 2018;Schlick-Steiner et al. 2010). Based on such integrative taxonomy, new bird taxa have been recently described (Alström et al. 2016;Stervander et al. 2020) and taxonomic rearrangements have been proposed, e.g. in pittas (Irestedt et al. 2013), bush warblers, prinias (Alström et al. 2020), larks (Alström et al. 2021), babblers (Gwee et al. 2020;Renner et al. 2017), and bulbuls (Garg et al. 2016). ...
... The ancestral range reconstructions indicated that the ancestor of Clade II (Desmoxytes + Nagaxytes + Spinaxytes) in the Tenasserim Range dispersed through the narrow part 'Isthmus of Kra' down to southern Thailand and then later evolved in the lower part of the Malay Peninsula multiple times by vicariance, probably coinciding with a period of the global sea-level fluctuation in this region (Woodruff 2003, Miller et al. 2005, Woodruff and Turner, 2009, Irestedt et al. 2013. The larger or smaller land area associated with the changes of sea level may have promoted terrestrial dispersal and vicariance across the region (de Bruyn et al. 2014, Jiang et al. 2019. ...
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