Phylogeography of a Successful Aerial Disperser: the Golden Orb Spider Nephila on Indian Ocean Islands Kuntner and Agnarsson

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Phylogeography of a Successful Aerial Disperser: the Golden Orb Spider Nephila on Indian Ocean Islands Kuntner and Agnarsson Phylogeography of a successful aerial disperser: the golden orb spider Nephila on Indian Ocean islands Kuntner and Agnarsson Kuntner and Agnarsson BMC Evolutionary Biology 2011, 11:119 http://www.biomedcentral.com/1471-2148/11/119 (9 May 2011) Kuntner and Agnarsson BMC Evolutionary Biology 2011, 11:119 http://www.biomedcentral.com/1471-2148/11/119 RESEARCHARTICLE Open Access Phylogeography of a successful aerial disperser: the golden orb spider Nephila on Indian Ocean islands Matjaž Kuntner1,2* and Ingi Agnarsson1,2,3 Abstract Background: The origin and diversification patterns of lineages across the Indian Ocean islands are varied due to the interplay of the complex geographic and geologic island histories, the varying dispersal abilities of biotas, and the proximity to major continental landmasses. Our aim was to reconstruct phylogeographic history of the giant orbweaving spider (Nephila) on western Indian Ocean islands (Madagascar, Mayotte, Réunion, Mauritius, Rodrigues), to test its origin and route of dispersal, and to examine the consequences of good dispersal abilities for colonization and diversification, in comparison with related spiders (Nephilengys) inhabiting the same islands, and with other organisms known for over water dispersal. We used mitochondrial (COI) and nuclear (ITS2) markers to examine phylogenetic and population genetic patterns in Nephila populations and species. We employed Bayesian and parsimony methods to reconstruct phylogenies and haplotype networks, respectively, and calculated genetic distances, fixation indices, and estimated clade ages under a relaxed clock model. Results: Our results suggest an African origin of Madagascar Nephila inaurata populations via Cenozoic dispersal, and the colonization of the Mascarene islands from Madagascar. We find evidence of gene flow across Madagascar and Comoros. The Mascarene islands share a common ‘ancestral’ COI haplotype closely related to those found on Madagascar, but itself absent, or as yet unsampled, from Madagascar. Each island has one or more unique haplotypes related to the ancestral Mascarene haplotype. The Indian Ocean N. inaurata are genetically distinct from the African populations. Conclusions: Nephila spiders colonized Madagascar from Africa about 2.5 (0.6-5.3) Ma. Our results are consistent with subsequent, recent and rapid, colonization of all three Mascarene islands. On each island, however, we detected unique haplotypes, consistent with a limited gene flow among the islands subsequent to colonization, a scenario that might be referred to as speciation in progress. However, due to relatively small sample sizes, we cannot rule out that we simply failed to collect Mascarene haplotypes on Madagascar, a scenario that might imply human mediated dispersal. Nonetheless, the former interpretation better fits the available data and results in a pattern similar to the related Nephilengys. Nephilengys, however, shows higher genetic divergences with diversification on more remote islands. That the better disperser of the two lineages, Nephila, has colonized more islands but failed to diversify, demonstrates how dispersal ability can shape both the patterns of colonization and formation of species across archipelagos. Background the complex geographic andgeologichistoryofthe Oceanic islands are convenient models for studying dis- islands, the varying dispersal abilities of local biotas, and persal of biotas and for understanding how dispersal abil- the proximity to major continental landmasses, Africa and ity relates to speciation [1]. Questions concerning the Asia, with dramatically different biotas. Madagascar, for origination and diversification of lineages across the Indian example contains both the lineages of vicariant origin and Ocean islands are fascinating because of the interplay of those arriving via more recent Cenozoic dispersal, and a mixture of African, Asian, and even Australasian elements * Correspondence: [email protected] [2-4]. Some other smaller volcanic islands, in turn, only 1Institute of Biology, Scientific Research Centre, Slovenian Academy of contain lineages that have dispersed there, but the source Sciences and Arts, Novi trg 2, P. O. Box 306, SI-1001 Ljubljana, Slovenia landmasses may be diverse including the above mentioned Full list of author information is available at the end of the article © 2011 Kuntner and Agnarsson; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Kuntner and Agnarsson BMC Evolutionary Biology 2011, 11:119 Page 2 of 9 http://www.biomedcentral.com/1471-2148/11/119 continents, as well as Madagascar, and other islands. The Table 1 Major landmasses and islands occupied by Nephil distribution and diversity of lineages across volcanic a and Nephilengys islands will, to a large degree, be a function of dispersal Landmasses and islands Nephila Nephilengys ability of lineages, with better dispersers occupying more North America y of the islands. However, the fact that good dispersers Central America y occur on more islands does not necessarily mean that they South America y y are also more diverse across archipelagos. One of the key Cuba y questions surrounding dispersal is to ‘determine the Hispaniola y impact of dispersal distances and [for spiders] ballooning Puerto Rico y propensity on gene flow and speciation...” [5]. Gene flow is Lesser Antilles y more rapidly disrupted in poor dispersers because even Eurasia y y narrow barriers can be effective isolators [6,7]. Hence, pro- Africa y y cesses of allopatric speciation are expected to start operat- Cape Verde y ing earlier in poor dispersers. Sao Tome y y Many spiders are excellent dispersers, such that they Socotra y have colonized and diversified across archipelagos world- Seychelles y y wide. Therefore, spiders have played a prominent role as Aldabra y y study organisms in the island diversification and biogeo- Comoros (incl. Mayotte) y y graphy [8-16]; however, none of these studies had a focus Madagascar y y on the Indian Ocean apart from Madagascar and Comoros Réunion y y [10,17]. Here we study a lineage of an excellent disperser, Mauritius y y the giant golden orb weaving spiders (genus Nephila), and Rodrigues y compare and contrast its colonization route, as well as the Sri Lanka y y distribution and diversity of this lineage with that of a Hainan y poorer disperser, its sister lineage Nephilengys [18]. The Taiwan y giant golden orb weaving spiders (genus Nephila) are dis- Japan y tributed pantropically and represent conspicuous elements Philippines y y of tropical terrestrial invertebrate faunas [19]. Compared Singapore y y with Nephilengys, Nephila species are much more wide- Sumatra y y spread (Table 1) having colonized most land masses Java y y except the most remote oceanic islands such as Hawaii, Sulawesi y y Galapagos, and Polynesia. Precise mechanisms of Nephila Lesser Sundas y y dispersal are not documented; however, orb weavers gen- Moluccas y erally disperse by wind travel termed ‘ballooning’ [5], New Guinea y y which is likely also true for Nephila [20]. Nephila popula- New Britain y tions are found on most islands of the Indian Ocean, e.g. Solomon Islands y Madagascar, the Comoro chain, Aldabra and Seychelles, as New Caledonia y well as the Mascarene archipelago, from Réunion through Australia y y Mauritius to Rodrigues (Figure 1) [21]. Tasmania y Recently, we investigated biogeographic and diversifica- New Zealand y tion patterns of Nephilengys in this region, and found that Vanuatu y its diversity had been underestimated [18]. We found that Fiji y the patterns of Nephilengys phylogenetic and population Tonga y genetic structure indicate a Cenozoic colonization of TOTAL 40 19 Madagascar from Africa, with a subsequent colonization Nephila is much more widespread, which suggests it is a better disperser of, and diversification in, more remote islands. Thus, two compared with its sister genus Nephilengys. Data from [18,21,61] and http:// of the three volcanic Mascarene islands, Réunion and www.nephilidae.com. Mauritius, harbour an endemic species each, whereas the populations on Mayotte (part of the Comoro chain) are endemic species, N. ardentipes Butler, 1876, differing from intermixed with those on Madagascar. Compared to N. inaurata in female habitus (Figure 2) and in other mor- Nephilengys, Nephila inhabits one additional island in the phological features [19]. Other target populations purport- Mascarenes, namely Rodrigues, a small and isolated volca- edly belong to N. inaurata (Walckenaer, 1842), a species nic island (109 km2, 560 km east of Mauritius; Figure 1). widespread from the eastern African coast to the islands On Rodrigues, Nephila is thought to be represented by an of the Indian Ocean [19,21,22]. However, the species Kuntner and Agnarsson BMC Evolutionary Biology 2011, 11:119 Page 3 of 9 http://www.biomedcentral.com/1471-2148/11/119 Africa LEGEND Mayotte Antananarivo Perinet Comoros N=1 Reunion N=2 N=4 N=1 N=4 Mauritius N=1 N=1 Rodrigues Madagascar Mascarenes N=3 1000 km N=1 N=1 N=12 N=2 N=11 N=19 N=1 N=8 N=1 N=1 N=2 N=1 N=2 ITS2 N=4 N=1 CO1 N=1 Figure 1 Area of study with sampling localities and haplotype networks (ITS2, CO1) of Nephila populations. The latter are consistent with one species inhabiting the islands of the western Indian Ocean, but in the process of speciating, e.g. on Rodrigues. Islands are colour coded, and the size of each haplotype is proportional to the number of individuals sharing it. Lines connect haplotypes through inferred substitution events (dots). status of both N. inaurata and N. ardentipes requires test- would exhibit a higher level of gene flow among these ing with molecular data. islands. Finally, we were interested in comparing the bio- Within this study, we were interested in a comparison geographic patterns of Nephila on the Indian Ocean of biogeography and diversification patterns between islands with those of other aerially dispersed organisms, Nephila and Nephilengys onthesameislandsinthe in order to detect common causes [23].
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