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Divergence of Island Biotas When They Were Not Always Islands ISSN 1948‐6596 news and update update Divergence of island biotas when they were not always islands Islands have frequently captured the attention of species (Kallimanis et al. 2010), and divergence biogeographers, providing insights into oceanic resulting from the development of island‐ dispersal capabilities (McDowall 2002), the proc‐ mainland allopatric distributions is typically in‐ esses of adaptation and diversification (Darwin voked (Fig. 1a). However, continental shelf islands 1872, Losos and Ricklefs 2009), and immigration‐ have repeatedly and predominantly experienced extinction dynamics (MacArthur and Wilson terrestrial connections to mainlands throughout 1967). Furthermore, the presence of related but the Pleistocene, represented by glacial low sea distinct lineages on islands and continents is con‐ stands (Lambeck et al. 2002). Therefore, the diver‐ sidered to represent classic examples of allopatric gence of continental shelf island biotas from those speciation (Mayr 1942). However, for continental on the mainland may have occurred by various shelf islands—those that possessed terrestrial means (allopatric, peripatric, parapatric or sym‐ connections to other landmasses via exposed con‐ patric speciation; Coyne and Orr 2004) prior to the tinental shelf during low sea stands (Whittaker development of island‐mainland allopatric distri‐ and Fernández‐Palacios 2007)—the interpretation butions themselves (e.g. Fig. 1b,c). may not always be so simple. A recent study from Taiwan illustrates a Continental shelf islands are common novel approach by which the divergence of sister throughout the globe, ranging from the numerous lineages can be tested for deviation from a strictly small nearshore islands that dot our coastlines, to allopatric island‐mainland model. Li et al. (2010a) larger and more notable examples, represented studied Taiwanese and Chinese hwamei by places such as Tasmania, New Guinea, Borneo, (Leucodioptron taewanus and L. canorum Sri Lanka, Taiwan, Japan, England and the Falkland canorum, respectively), representing species of Islands (Malvinas). Continental shelf islands, like babbler that are sedentary and occupy the mar‐ oceanic islands, often house a variety of endemic gins of secondary broadleaf evergreen woodlands. Figure 1. Hypothetical divergence scenarios leading to contemporary island‐mainland sister‐lineages. Cir‐ cles of different colours indicate the geographic distribution of diverging lineages. The grey shaded areas indi‐ cate continental shelf exposed dur‐ ing Pleistocene glaciations between China and the continental shelf is‐ land of Taiwan. (a) Strict island‐ mainland allopatric divergence. Is‐ land and mainland populations of a widespread ancestor were isolated following a marine transgression. (b) Divergence under gene flow. Diver‐ gence of lineages occurred despite sympatry or parapatry and gene flow, with island‐mainland allopatric distributions formed subsequently. (c) Divergence of lineages within a region (allopatric within the mainland, in this case), with island‐ mainland allopatry formed subse‐ quently. frontiers of biogeography 3.4, 2012 — © 2012 the authors; journal compilation © 2012 The International Biogeography Society 125 news and update These species are unlikely candidates for marine elevated sea levels (Raymo et al. 2011), and there‐ dispersal, but movement between Taiwan and fore divergence must have been occurring within China may have been achieved by their ancestors either Taiwan or China, and not across both. Sec‐ during Pleistocene low sea stands, when the Tai‐ ondly, as a population of L. c. canorum artificially wan Strait was emergent (Fig. 1). Consequently, introduced to Taiwan can interbreed with L. tae‐ divergence of these lineages may have proceeded wanus (Li et al. 2010b), the cessation of gene flow under an alternate geographic scenario. 0.52 Mya must represent the formation of an on‐ Li et al. (2010a) documented DNA sequence going allopatric distribution. Li et al. (2010a) variation at a large number of independent nu‐ looked to paleovegetation reconstructions and clear markers (18 loci), and employed these data the presence of unsuitable hwamei habitat to test hypotheses regarding the demographic (savannah) across the Taiwan Strait during the last history of lineages using weighted‐regression‐ glacial period as a potential explanation for a lack based approximate Bayesian computations. Two of more recent gene flow. Regardless, the forma‐ models of lineage divergence were compared for tion of an allopatric island‐mainland distribution the hwamei. The first represented divergence un‐ appears only to have interrupted gene flow be‐ der strict allopatry (without subsequent gene tween lineages that were already diverging in flow), akin to a single colonisation (founder) parapatry or sympatry. event, or vicariant isolation of populations (Fig. The above example highlights the potential 1a). The alternate model allowed gene flow for a complexities of historical divergence between period subsequent to the initiation of lineage di‐ continental shelf island and mainland populations. vergence, consistent with divergence under para‐ Such complexity may owe to the geographically patry or sympatry and interbreeding (Fig. 1b). peripheral location of continental shelf islands, Coalescent simulations were performed under placing them ideally to sequester variants that these models, and 11 summary statistics were developed in a mainland species (e.g. Fig. 1c). Re‐ calculated for each simulated 18‐locus dataset gardless, allopatric island‐mainland divergence of (e.g. number of polymorphic sites, haplotype di‐ lineages should not be assumed for continental versity, nucleotide diversity, FST, number of poly‐ island biotas, and further research is required to morphisms that are shared, unique, or fixed be‐ examine the prevalence of alternate divergence tween lineages). The summary statistics from scenarios. The same could also be said for other simulated datasets were then compared against systems where allopatric divergence is typically those from the empirical data. The non‐allopatry invoked (e.g. oceanic islands); instead, divergence (gene flow following divergence) model better may have occurred during periods of on‐going explained the observed data than the strict allo‐ gene flow (“soft vicariance”; Hickerson and Meyer patry model. A large time discrepancy was also 2008), or preceded the attainment of contempo‐ observed between the initiation of lineage diver‐ rary allopatric distributions. gence (3.47 Mya) and cessation of gene flow (0.52 Mya). Christopher Paul Burridge The estimates of total lineage divergence School of Zoology, University of Tasmania, Hobart, Australia. time, and time for cessation of gene flow, raise e‐mail: [email protected]; http://fcms.its.utas.edu.au/ two interesting questions regarding the geo‐ scieng/zoo/pagedetails.asp?lpersonId=5232 graphic distributions of these lineages during their divergence (assuming that these time estimates References are not strongly influenced by potential errors Coyne, J.A. & Orr, H.A. (2004) Speciation. Sinauer Asso‐ with the molecular clocks). Firstly, although a ciates, Sunderland, Massachusetts. model involving gene flow between lineages dur‐ Darwin, C. (1872) The origin of species by means of ing the early stages of their divergence was fa‐ natural selection, or the preservation of fa‐ voured, the mid‐Pliocene was characterised by voured races in the struggle for life. John Murray, London. 126 © 2012 the authors; journal compilation © 2012 The International Biogeography Society — frontiers of biogeography 3.4, 2012 ISSN 1948‐6596 news and update Hickerson, M. & Meyer, C. (2008) Testing comparative Losos, J.B. & Ricklefs, R.E. (2009) Adaptation and diver‐ phylogeographic models of marine vicariance sification on islands. Nature, 457, 830‐836. and dispersal using a hierarchical Bayesian ap‐ MacArthur, R.H. & Wilson, E.O. (1967) The theory of proach. BMC Evolutionary Biology, 8, 322. island biogeography. Princeton University Press, Kallimanis, A.S., Bergmeier, E., Panitsa, M., Georghiou, Princeton, New Jersey. K., Delipetrou, P. & Dimopoulos, P. (2010) Bio‐ Mayr, E. (1942) Systematics and the origin of species, geographical determinants for total and en‐ from the viewpoint of a zoologist. Columbia demic species richness in a continental archipel‐ University Press, New York. ago. Biodiversity and Conservation, 19, 1225‐ McDowall, R.M. (2002) Accumulating evidence for a 1235. dispersal biogeography of southern cool tem‐ Lambeck, K., Esat, T.M. & Potter, E.‐K. (2002) Links be‐ perate freshwater fishes. Journal of Biogeogra‐ tween climate and sea levels for the past three phy, 29, 207‐219. million years. Nature, 419, 199‐206. Raymo, M.E., Mitrovica, J.X., O'Leary, M.J., DeConto, Li, J.‐W., Yeung, C.K.L., Tsai, P.‐W., et al. (2010a) Reject‐ R.M. & Hearty, P.J. (2011) Departures from ing strictly allopatric speciation on a continental eustasy in Pliocene sea‐level records. Nature island: prolonged postdivergence gene flow be‐ Geoscience, 4, 328‐332. tween Taiwan (Leucodioptron taewanus, Whittaker, R.J. & Fernández‐Palacios, J.M. (2007) Island Passeriformes Timaliidae) and Chinese (L. biogeography. Ecology, evolution and conserva‐ canorum canorum) hwameis. Molecular Ecology, tion. Oxford University Press, Oxford. 19, 494‐507. Li, S.‐H., Yeung, C.K.L., Han, L., Manh Hung, L., Wang, C. Edited by Spyros Sfenthourakis ‐X., Ding, P. & Yao, C.‐T. (2010b) Genetic intro‐ gression between an introduced babbler,
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