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Phylogeography and Genetic Diversity of a Widespread Old World Butterfly, Lampides Boeticus (Lepidoptera: Lycaenidae)

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Phylogeography and Genetic Diversity of a Widespread Old World Butterfly, Lampides Boeticus (Lepidoptera: Lycaenidae) BMC Evolutionary Biology BioMed Central Research article Open Access Phylogeography and genetic diversity of a widespread Old World butterfly, Lampides boeticus (Lepidoptera: Lycaenidae) David J Lohman*1, Djunijanti Peggie2, Naomi E Pierce3 and Rudolf Meier1 Address: 1Department of Biological Sciences, National University of Singapore, 14 Science Drive 4, Singapore 117543, Republic of Singapore, 2Division of Zoology, Research Centre for Biology-LIPI, Jl. Raya Jakarta-Bogor Km. 46, Cibinong-Bogor 16911, Indonesia and 3Museum of Comparative Zoology, Harvard University, 26 Oxford St., Cambridge, Massachusetts 02138, USA Email: David J Lohman* - [email protected]; Djunijanti Peggie - [email protected]; Naomi E Pierce - [email protected]; Rudolf Meier - [email protected] * Corresponding author Published: 30 October 2008 Received: 21 April 2008 Accepted: 30 October 2008 BMC Evolutionary Biology 2008, 8:301 doi:10.1186/1471-2148-8-301 This article is available from: http://www.biomedcentral.com/1471-2148/8/301 © 2008 Lohman et al; 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. Abstract Background: Evolutionary genetics provides a rich theoretical framework for empirical studies of phylogeography. Investigations of intraspecific genetic variation can uncover new putative species while allowing inference into the evolutionary origin and history of extant populations. With a distribution on four continents ranging throughout most of the Old World, Lampides boeticus (Lepidoptera: Lycaenidae) is one of the most widely distributed species of butterfly. It is placed in a monotypic genus with no commonly accepted subspecies. Here, we investigate the demographic history and taxonomic status of this widespread species, and screen for the presence or absence of the bacterial endosymbiont Wolbachia. Results: We performed phylogenetic, population genetic, and phylogeographic analyses using 1799 bp of mitochondrial sequence data from 57 specimens collected throughout the species' range. Most of the samples (>90%) were nearly genetically identical, with uncorrected pairwise sequence differences of 0 – 0.5% across geographic distances > 9,000 km. However, five samples from central Thailand, Madagascar, northern Australia and the Moluccas formed two divergent clades differing from the majority of samples by uncorrected pairwise distances ranging from 1.79 – 2.21%. Phylogenetic analyses suggest that L. boeticus is almost certainly monophyletic, with all sampled genes coalescing well after the divergence from three closely related taxa included for outgroup comparisons. Analyses of molecular diversity indicate that most L. boeticus individuals in extant populations are descended from one or two relatively recent population bottlenecks. Conclusion: The combined analyses suggest a scenario in which the most recent common ancestor of L. boeticus and its sister taxon lived in the African region approximately 7 Mya; extant lineages of L. boeticus began spreading throughout the Old World at least 1.5 Mya. More recently, expansion after population bottlenecks approximately 1.4 Mya seem to have displaced most of the ancestral polymorphism throughout its range, though at least two early-branching lineages still persist. One of these lineages, in northern Australia and the Moluccas, may have experienced accelerated differentiation due to infection with the bacterial endosymbiont Wolbachia, which affects reproduction. Examination of a haplotype network suggests that Australia has been colonized by the species several times. While there is little evidence for the existence of morphologically cryptic species, these results suggest a complex history affected by repeated dispersal events. Page 1 of 14 (page number not for citation purposes) BMC Evolutionary Biology 2008, 8:301 http://www.biomedcentral.com/1471-2148/8/301 Background and garden peas (Pisum sativum) are among its preferred The study of speciation lies at the nexus of micro- and host plants, and the butterfly is a crop pest in many parts macroevolution, i.e., phylogenetics and population genet- of its range [4]. Lampides boeticus is among the approxi- ics. Phylogeography, which incorporates both approaches mately three-quarters of butterfly species in the family in a geographical context, examines the role of different Lycaenidae that associate with ants as larvae and pupae historical processes in population demography, differen- [5]. The species is facultatively tended by a variety of ants tiation and speciation [1]. The advent of rapid and afford- throughout its range, including Camponotus spp., Irid- able DNA sequencing over the past 15 years has catalyzed omyrmex spp., and 'tramp' ant species including Tapinoma studies on the evolutionary dynamics of populations and melanocephalum and the Argentine ant, Linepithema humile the discovery of previously unrecognized morphologi- [6,7]. cally cryptic species [2]. We sampled 57 L. boeticus from 39 localities on four con- The pea blue butterfly, Lampides boeticus (L.) (Lepidoptera: tinents (Fig. 1) to test the hypothesis that this widespread Lycaenidae), is one of the most widely distributed butter- species, as currently circumscribed, consists of more than flies in the world, and is currently found across the Palae- one genetically distinct taxon. We also used nucleotide arctic region from Britain to Japan, throughout suitable sequence data to further examine the genetic structure of habitat in Africa, Madagascar, South East Asia, and Aus- this species and analyze the demographic history of the tralia, extending eastwards to parts of Oceania including sampled populations. Hawaii. It occurs in temperate, subtropical, and tropical biomes in both lowland and montane localities, typically Results in open and/or disturbed areas. Phylogenetic analyses and node dating Bayesian, maximum likelihood and parsimony phyloge- Taxonomically, L. boeticus is the only species in its genus netic analyses arrived at similar phylogenetic hypotheses and has no commonly recognized subspecies, despite its for the evolutionary history of L. boeticus that agreed on all wide distribution. The larval stages feed on plants in at major groupings (Fig. 2B). Cytochrome c oxidase subunit I least six families, although Leguminosae (particularly (COI) had 48 variable sites and cytochrome b (cytB) had Papilionoideae) is the predominant host plant taxon [3]. 28, of which 35 and 17 were parsimoniously informative, Cultivated legumes, including broad beans (Vicia faba) respectively. Thus, cytB was more variable – 5.35% of 2 3 1 4 5 WESTERN EASTERN 51-52 PALAEARCTIC 6 7 PALAEARCTIC 48-49 50 47 INDO- BURMESE 36-37 34-35 45-46 33 43-44 38-42 PHILIPPINE 32 30-31 AFRICAN 11 17-18 WALLACEAN 10 9 27 8 19-20 21-22 26 SUNDAIC 23 28-29 53 24-25 14-16 12 56 MALAGASY 57 AUSTRALIAN 55 13 54 MapFigure of Lampides1 boeticus collection localities Map of Lampides boeticus collection localities. Numbers refer to sample information in Table 1. Different colors distin- guish labeled biogeographic regions. Page 2 of 14 (page number not for citation purposes) BMC Evolutionary Biology 2008, 8:301 http://www.biomedcentral.com/1471-2148/8/301 nucleotide sites were variable across all samples – than analyses (Fig. 2B). Lampides boeticus was monophyletic COI, in which 4.10% of nucleotide sites varied. The per- with regard to the three chosen outgroup species. In addi- centage of parsimoniously informative nucleotide sites tion to the divergent genotypes in clades C and D (Fig. was also higher in cytB (3.28% vs. 2.87%), as was the 2B), there were two other groups that were supported by number of nucleotide sites with parsimoniously informa- Bayesian, maximum likelihood and parsimony analyses. tive non-synonymous substitutions (3 vs. 0). The parsi- Clade A contained all haplotypes from Africa, Madagas- mony analysis resulted in 1,130 most parsimonious trees car, the eastern and western Palaearctic, Indo-Burma, and with a tree score of 336. The strict consensus of these trees the Philippines not found in the divergent clades C and D. differed with regard to two nodes when compared to the Grade B is a paraphyletic assemblage containing all of the tree obtained in both Bayesian and maximum likelihood haplotypes from the Sundaland, Wallacean, and Austral- 3 4 A 7 1,2,5,6,8,10,12,14,35,36,37 3 4 11 13 9 34 1,2,5,6,8,10,12,14,35,36,37 11 15 80,59 13 65,67 32 49 9 15 44 clade A 45 38 7 39,41,42,43,47,48,51 38 99,57 46 44,45,46,50 68,63 40 52 50 39,41,42,43,47,48,51 40 54 22 55,52 17 34 19 18,21,23 30,31 <50,<50 32 20 52 55 57 70,67 49 53 25,27,28,29 77,79 17,19,20 22 54, 54 18,21,23 <50,<50 30,31 25,27,28,29 grade B III 53 54 B 55 100,100 II 57 100,100 16 100,100 clade C 99,100 33 99,93 I 0.1 substitutions/site 24,26 69,70 89,84 clade D 56 100,100 Cacyreus marshalli Uranothauma falkensteini Phlyaria cyara RelationshipsFigure 2 among COI+cytB mitochondrial haplotypes of Lampides boeticus Relationships among COI+cytB mitochondrial haplotypes of Lampides boeticus. Numbers refer to sample informa- tion in Table 1; colors denote biogeographic regions designated in Fig. 1. A. Most parsimonious haplotype network of L. boeti- cus constructed with 99% connection limit. Black circles indicate extinct or unsampled haplotypes that differ by one nucleotide substitution from the adjoining haplotype. B. Bayesian consensus tree of L. boeticus haplotypes. Numbers above braches indi- cate Bayesian posterior probability and maximum likelihood bootstrap support, respectively; numbers below indicate parsi- mony bootstrap symmetric resampling and jackknife support, respectively, for parsimony analyses that resulted in a topologically similar tree. Estimated node ages: I, 6.9 ± 0.6 My; II, 1.5 ± 0.2 My; III, 1.4 ± 0.2 My Page 3 of 14 (page number not for citation purposes) BMC Evolutionary Biology 2008, 8:301 http://www.biomedcentral.com/1471-2148/8/301 ian regions not found clades C and D.
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