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Systematics of Polistes (Hymenoptera: Vespidae), with a Phylogenetic Consideration of Hamilton’S Haplodiploidy Hypothesis

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Systematics of Polistes (Hymenoptera: Vespidae), with a Phylogenetic Consideration of Hamilton’S Haplodiploidy Hypothesis Ann. Zool. Fennici 43: 390–406 ISSN 0003-455X Helsinki 29 December 2006 © Finnish Zoological and Botanical Publishing Board 2006 Systematics of Polistes (Hymenoptera: Vespidae), with a phylogenetic consideration of Hamilton’s haplodiploidy hypothesis Kurt M. Pickett*, James M. Carpenter & Ward C. Wheeler Division of Invertebrate Zoology, American Museum of Natural History, Central Park West at 79th Street, New York, NY 10023, USA * Current address: Department of Biology, University of Vermont, Room 120A Marsh Life Science Building, 109 Carrigan Drive, Burlington, VT 05405, USA Received 30 Nov. 2005, revised version received 21 Nov. 2006, accepted 4 May 2006 Pickett, K. M., Carpenter, J. M. & Wheeler, W. C. 2006: Systematics of Polistes (Hymenoptera: Vespidae), with a phylogenetic consideration of Hamilton’s haplodiploidy hypothesis. — Ann. Zool. Fennici 43: 390–406. A review of previously published cladistic analyses of Polistes is presented. The two most recent analyses of Polistes are shown to be largely consistent phylogenetically. Although the taxonomy implied by each differs, this difference is shown to be mostly due to taxon sampling. After the review, a phylogenetic analysis of Polistes — the most data-rich yet undertaken — is presented. The analysis includes new data and the data from previously published analyses. The differing conclusions of the previous studies are discussed in light of the new analysis. After discussing the status of subge- neric taxonomy in Polistes, the new phylogeny is used to test an important hypothesis regarding the origin of social behavior: the haplodiploidy hypothesis of Hamilton. Prior phylogenetic analyses so while these studies achieved their goal, with within Polistes resolutions leading to rejection of Emery’s Rule, they had little to say about broader phylogenetic Cladistic analysis of species-level relationships patterns within the genus. within Polistes was first carried out with a lim- The first large-scale analysis within Polistes ited, specific objective: to determine relation- was Carpenter (1996), who studied the mor- ships among the socially parasitic inquiline phology of 144 species and an additional 43 species and their host species; that is, to test subspecies, thus sampling most of the diver- Emery’s Rule. Analyses of allozymes (Carpenter sity within the genus (presently 204 species et al. 1993) and COI sequence data (Choudhary and an additional 99 subspecies). He presented et al. 1994) thus treated nine species, the three three analyses of 33 morphological characters inquilines, their hosts, and outgroups. Analysis — first treating the 12 subgenera recognized of these data sources combined with morphol- by Richards (1973, 1978) as groundplan ter- ogy (Carpenter 1997) treated 11 species. The minals, then subdividing these into subgenera inquilines and their hosts are European, while and species groups invariant for informative the outgroups were North American species, characters (i.e., as summary terminals). Neither ANN. ZOOL. FENNICI Vol. 43 • Systematics of Polistes 391 Fig. 1. A map of COI, numbered according to its position within the complete Drosophila yakuba mitochondrial genome. The map indicates the primers and regions of COI employed in previous analyses (see text). of these first two analyses completely resolved 1979, Yamane & Okazawa 1981, Nelson 1982, relationships among these groups, but the second Kojima & Yamane 1984, Kojima & Keeping did show that the New World subgenus Aph- 1985, Kojima 1987), and with characters of anilopterus was paraphyletic in terms of the nest architecture from Wenzel (1993). In the subgenera Epicnemius, Fuscopolistes, Onerar- combined analysis, as with Carpenter (1996) the ius, and Palisotius (all from the New World clade for the New World species of Polistes was as well). In addition, this analysis found Epic- monophyletic, as were each of the Old World nemius to be paraphyletic in terms of Onerar- subgenera. However, among the Old World taxa ius, Palisotius and Fuscopolistes. The analysis Polistes s. str. was more basal than Polistella and also established all the New World species as Gyrostoma (Megapolistes). Moreover, within the a monophyletic lineage. Accordingly, Carpen- New World clade, both Aphanilopterus s. str. and ter (1996) synonymized Epicnemius, Onerarius, Epicnemius were monophyletic (however, the Palisotius, and Fuscopolistes with Aphanilop- species sample was respectively just ten and two terus (henceforth Aphanilopterus; cf. Aphanilop- species). terus sensu Richards, henceforth Aphanilopterus Pickett and Wenzel (2004) subsequently s. str.). Thus Aphanilopterus in the present sense analyzed 40 species of Polistes (33 of which is a monophyletic subgenus. Carpenter (1996) were Aphanilopterus spp.) using slightly modi- also synonymized the subgenera Polistella with fied morphological data and a different, non- Stenopolistes, Polistes s. str. with Sulcopolistes, overlapping fragment of COI (Fig. 1). As with and Gyrostoma with Megapolistes, in each case the preceding studies, the New World species after demonstrating paraphyly. A third analysis of Polistes formed a monophyletic group. The by Carpenter (1996) of the four subgenera result- arrangement among the Old World subgenera ing after synonymy of both New World and Old was different from both of the previous studies, World subgenera did not resolve relationships but was based on just five species. In contrast to among Gyrostoma and Polistella, but did show a the study by Arévalo et al. (2004), the results of sister-group relationship between Polistes s. str. Pickett and Wenzel (2004) agreed with Carpen- and Aphanilopterus. ter’s (1996) conclusions that neither Aphanilop- The first extensive molecular treatment was terus s. str. nor Epicnemius are monophyletic. by Arévalo et al. (2004), which included 33 spe- Pickett and Wenzel (2004) also indicated para- cies of Polistes, along with 33 species of other phyly of Fuscopolistes, which had not been sug- tribes of Polistinae. The molecular data consisted gested by previous work. of mitochondrial COI sequences, three nuclear It may seem unexpected that the same locus DNA microsatellite flanking sequences, and the (COI) might support different topologies. This three repeat motifs for the microsatellites repre- finding, though, is not surprising when it is real- sented by gap-coding. These data were combined ized that the process of evolution can change with the adult morphological characters of Car- through time, even within a single locus. This penter (1996), with characters used by Carpenter phenomenon of heterotachy (Lopez et al. 2002), et al. (2000) in their study of the genus Polybia, in which rates of evolution change both across with larval characters taken from Kojima (1998) and within sites, is known to occur in many loci, supplemented by other literature sources (Reid especially those that are protein-coding (e.g. 1942, Dias Filho 1975, Wheeler & Wheeler Fitch 1976). COI itself has recently been shown 392 Pickett et al. • ANN. ZOOL. FENNICI Vol. 43 to exhibit statistically significant heterotachy in ing” below), adult morphological data as modi- lineages of social wasps (Pickett et al. 2005). fied from Pickett and Wenzel (2004) and larval Further, the half of the gene closest to the 5´ end data from the literature (partly used by Arévalo exhibits more heterotachy than the half near the et al. 2004; see below); the Pickett and Wenzel 3´ end, and that heterotachy is exhibited differ- (2004) morphology set was chosen over that in entially across the lineages (i.e., some branches Arévalo et al. (2004) because the latter data were exhibit heterotachy in part of the gene, but not compiled so as to represent variability across the in others; Pickett et al. 2005). With this in mind, Polistinae, whereas the dataset of Pickett and the different results obtained by Arévalo et al. Wenzel (2004) was constructed to capture vari- (2004) and Pickett and Wenzel (2004) are not so ability within Polistes. After presentation of the unexpected after all. simultaneous analysis (Kluge 1989, Nixon and Even considering issues of heterotachy, how- Carpenter 1996), we use the resulting phylogeny ever, close examination of the topologies offered to investigate an historically important hypoth- by Arévalo et al. (2004) and Pickett and Wenzel esis of social evolution. (2004) reveal less conflict than their differing taxonomic findings suggest. While it is true that Arévalo et al. (2004) found two subgenera to be Materials and methods monophyletic while Pickett and Wenzel (2004) did not, this is due mainly to differential taxo- In all, we treat 48 taxa (see Appendix). These nomic sampling within Polistes. For example, include all Polistes species from Arévalo et al. Arévalo et al. (2004) report that Fuscopolistes (2004) and all taxa, both species and subspe- is monophyletic, whereas Pickett and Wenzel cies, from Pickett and Wenzel (2004) save those (2004) found it polyphyletic, in the form of two with substantial gaps in the molecular data (see well-separated clades. One of the clades in Pick- below). ett and Wenzel (2004) comprised three taxa (P. flavus, P. poeyi, and P. perplexus) not included in the Arévalo et al. (2004) analysis. As such, Morphological data had these taxa been omitted from Pickett and Wenzel, that study too would have reported the The morphological data all derive from data monophyly of Fuscopolistes. Also, if the pre- matrices used in previously published analyses, ferred cladogram from Pickett and Wenzel (fig. with adult morphology
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