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A Molecular Phylogeny for the Tribe Dacini (Diptera: Tephritidae): Systematic and Biogeographic Implications

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A Molecular Phylogeny for the Tribe Dacini (Diptera: Tephritidae): Systematic and Biogeographic Implications This may be the author’s version of a work that was submitted/accepted for publication in the following source: Krosch, Matthew, Schutze, Mark, Armstrong, Karen, Graham, Glenn, Yeates, David, & Clarke, Anthony (2012) A molecular phylogeny for the Tribe Dacini (Diptera: Tephritidae): System- atic and biogeographic implications. Molecular Phylogenetics and Evolution, 64(3), pp. 513-523. This file was downloaded from: https://eprints.qut.edu.au/52922/ c Consult author(s) regarding copyright matters This work is covered by copyright. Unless the document is being made available under a Creative Commons Licence, you must assume that re-use is limited to personal use and that permission from the copyright owner must be obtained for all other uses. If the docu- ment is available under a Creative Commons License (or other specified license) then refer to the Licence for details of permitted re-use. It is a condition of access that users recog- nise and abide by the legal requirements associated with these rights. If you believe that this work infringes copyright please provide details by email to [email protected] License: Creative Commons: Attribution-Noncommercial-No Derivative Works 2.5 Notice: Please note that this document may not be the Version of Record (i.e. published version) of the work. Author manuscript versions (as Sub- mitted for peer review or as Accepted for publication after peer review) can be identified by an absence of publisher branding and/or typeset appear- ance. If there is any doubt, please refer to the published source. https://doi.org/10.1016/j.ympev.2012.05.006 1 A MOLECULAR PHYLOGENY FOR THE TRIBE DACINI (DIPTERA: TEPHRITIDAE): SYSTEMATIC 2 AND BIOGEOGRAPHIC IMPLICATIONS 3 4 Matthew N. Krosch1, Mark K. Schutze1,2, Karen F. Armstrong3, Glenn C. Graham4, David K. 5 Yeates5 and Anthony R. Clarke1,2 6 7 1. School of Earth, Environment and Biological Sciences, Science and Engineering Faculty, 8 Queensland University of Technology, G.P.O. Box 2434, Brisbane 4000, Queensland, 9 Australia. 10 2. CRC for National Plant Biosecurity, LPO Box 5012, Bruce 2617, A.C.T., Australia. 11 3. Bio-Protection Research Centre, PO Box 84, Lincoln University, Canterbury, New Zealand 12 4. Centre for Identification and Diagnostics, School of Life Sciences, The University of 13 Queensland, Brisbane 4072, Queensland, Australia 14 5. CSIRO Ecosystem Sciences, PO Box 1700, Canberra 2601, A.C.T., Australia 15 16 17 18 19 Abstract 20 With well over 700 species, the Tribe Dacini is one of the most species-rich clades within the 21 dipteran family Tephritidae, the true fruit flies. Nearly all Dacini belong to one of two very 22 large genera, Dacus Fabricius and Bactrocera Macquart. The distribution of the genera 23 overlap in or around the Indian subcontinent, but the greatest diversity of Dacus is in Africa 24 and the greatest diversity of Bactrocera is in south-east Asia and the Pacific. The monophyly 25 of these two genera has not been rigorously established, with previous phylogenies only 26 including a small number of species and always heavily biased to one genus over the other. 27 Moreover, the subgeneric taxonomy within both genera is complex and the monophyly of 28 many subgenera has not been explicitly tested. Previous hypotheses about the 29 biogeography of the Dacini based on morphological reviews and current distributions of 30 taxa have invoked an out-of-India hypothesis; however this has not been tested in a 31 phylogenetic framework. We attempted to resolve these issues with a dated, molecular 32 phylogeny of 125 Dacini species generated using 16S, COI, COII and white eye genes. The 33 phylogeny shows that Bactrocera is not monophyletic, but rather consists of two major 34 clades: Bactrocera s.s. and the ‘Zeugodacus group of subgenera’ (a recognised, but informal 35 taxonomic grouping of 15 Bactrocera subgenera). This ‘Zeugodacus’ clade is the sister group 36 to Dacus, not Bactrocera and, based on current distributions, split from Dacus before that 37 genus moved into Africa. We recommend that taxonomic consideration be given to raising 38 Zeugodacus to genus level. Supportive of predictions following from the out-of-India 39 hypothesis, the first common ancestor of the Dacini arose in the mid-Cretaceous 40 approximately 80mya. Major divergence events occurred during the Indian rafting period 41 and diversification of Bactrocera apparently did not begin until after India docked with 42 Eurasia (50-35mya). In contrast, diversification in Dacus, at approximately 65mya, 43 apparently began much earlier than predicted by the out-of-India hypothesis, suggesting 44 that, if the Dacini arose on the Indian plate, then ancestral Dacus may have left the plate in 45 the mid to late Cretaceous via the well documented India-Madagascar-Africa migration 46 route. We conclude that the phylogeny does not disprove the predictions of an out-of-India 47 hypothesis for the Dacini, although modification of the original hypothesis is required. 48 49 Keywords: Bactrocera, Dacus, Zeugodacus, phylogenetics, Gondwana 50 51 1.0 Introduction 52 The Tribe Dacini of the Tephritidae sub-family Dacinae contains approximately 770 53 described fruit fly species, as well as many undescribed species (Drew and Hancock, 2000). 54 The Dacini is considered monophyletic (Han and Ro, 2009) consisting of four genera; two 55 small genera, Ichneumonopsis Hardy (one sp) and Monacrostichus Bezzi (two spp), and two 56 very large genera, Dacus Fabricius (245 spp) and Bactrocera Macquart (528spp) (Drew and 57 Hancock, 2000). Both Dacus and Bactrocera are further subdivided into subgenera 58 (Bactrocera – ~30, Dacus - ~7, depending on source) (Drew, 1972, 1989; Hancock and Drew, 59 2006; White, 2006), and sometimes within those subgenera into species groups (Drew, 60 1989). Nearly all Dacus and Bactrocera species have frugivorous larvae and, although most 61 species are non-pest endemics of savannah areas (Dacus) or rainforests (Bactrocera) (Drew, 62 2004), a few species are horticultural pests of international importance (White and Elson- 63 Harris, 1992). 64 65 The distribution of the Dacini extends from Africa, where Dacus dominates, across India and 66 into Asia, Australia and the Pacific, where Bactrocera dominates (Drew, 2004). The greatest 67 generic and species diversity of Dacini occurs in south-east Asia (inclusive of India), where all 68 four genera are found (Ichneumonopsis and Monacrostichus are restricted to this region) 69 (Drew and Hancock, 1994b; Drew et al., 1998; Drew and Raghu, 2002; Drew and Romig, 70 2007). The presence of Dacini in Africa, Australia and India suggests the group may have 71 first evolved in Gondwana, but this is countered by the group’s much higher diversity in Asia 72 which suggests a Eurasian centre of origin. 73 74 Drew and Hancock (2000) and Drew (2004) have argued that the Dacini are of Gondwanan 75 rather than Eurasian origin, with the ancestral flies having originated on the Indian plate 76 after it rafted away from Gondwana. Once India docked with Eurasia around 50-35mya, 77 ancestral Dacus moved westward and diversified in Africa, while ancestral Bactrocera 78 moved eastward and diversified in the rainforests of south-east Asia and the Pacific. An 79 important part of the argument (as summarised in Fig 19.1 of Drew and Hancock, 2000) is 80 the subsequent movement of some Dacus species back into Asia and some Bactrocera 81 species, particularly members of the Zeugodacus group of subgenera, back into Africa. The 82 reasoning behind Drew and Hancock’s (2000) hypothesis is based on the absence of Dacini 83 in South America (hence diversification only beginning after Gondwana started breaking 84 up), the presence of basal genera (Ichneumonopsis and Monacrostichus) and subgenera 85 (e.g., B. (Tetradacus)) in south western Asia, and the abundance of more derived Dacus in 86 Africa and Bactrocera in south-east Asia, New Guinea and Australia. 87 88 Drew and Hancock’s (2000) hypothesis for the evolution of the Dacini, while developed 89 independently, is a ‘text book’ example of a general biogeographic pattern now known as 90 the ‘out-of-India’ hypothesis. The out-of-India hypothesis has been used to explain why 91 some clearly Gondwanan groups have high diversity in Asia and uses the same argument of 92 Drew and Hancock: i.e., groups of Gondwanan origin rafted on the Indian plate away from 93 Gondwana and then diversified following docking with Eurasia (Gower et al., 2002; Praveen 94 Karanth, 2006; Conti et al., 2007; Datta-Roy and Karanth, 2009; Svenson and Whiting, 2009; 95 Viseshakul et al., 2011). 96 97 While an out-of-India argument for the biogeography of the Dacini aligns with 98 biogeographic patterns seen in other plant and animal taxa, it is not the only hypothesis to 99 explain why a putative Gondwanan group may have high diversity in Asia. For other 100 Gondwanan taxa with Asian elements, arguments have also been made for out-of-Africa 101 (Masters et al., 2006; Surveswaran et al., 2010; Zhou et al., 2011) or out-of-Australia (Braby 102 et al., 2005; Braby and Pierce, 2007; Goldblatt et al., 2008; Cruaud et al., 2011) scenarios. 103 These hypotheses could also be applied to the Dacini, as could an out-of-Asia hypothesis 104 (Kosuch et al. 2001; Köhler & Glaubrecht 2007) if the group is not Gondwanan. Drew and 105 Hancock (2000) acknowledge that their Indian rafting hypothesis is dependent on there 106 being congruence between the timing of species diversification events and geological 107 events. What is also critical, but is unstated, is that their assumptions of Dacini phylogeny 108 (especially with respect to early-branching versus late-branching genera, sub-genera and 109 species) are correct. Independent molecular phylogenies, with estimated divergence times, 110 are needed to address these issues.
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