Molecular Phylogeny and Biogeography of the Spider Ants, Genus Leptomyrmex Mayr (Hymenoptera: Formicidae) ⇑ Andrea Lucky
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Molecular Phylogenetics and Evolution 59 (2011) 281–292 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Molecular phylogeny and biogeography of the spider ants, genus Leptomyrmex Mayr (Hymenoptera: Formicidae) ⇑ Andrea Lucky Department of Entomology, University of California, Davis, CA 95616, USA article info abstract Article history: This study provides the first phylogenetic reconstruction of the ant genus Leptomyrmex Mayr, a promi- Received 5 June 2010 nent endemic component of rain forest and wet sclerophyll forest in Australia, New Guinea and New Cal- Revised 17 February 2011 edonia. Five genes are used to reconstruct phylogeny and estimate of ages of diversification in order to Accepted 2 March 2011 test congruence of the history of nuclear and mitochondrial genes: three protein-coding nuclear genes: Available online 13 March 2011 arginine kinase (argK, 897 bp), long wavelength rhodopsin (LW Rh, 546 bp) and wingless (Wg, 409 bp), as well as the large subunit ribosomal gene 28S (482 bp) and the mitochondrial gene cytochrome oxidase Keywords: I (COI, 658 bp). Four different partitioning schemes were tested for optimal resolving power; results show Leptomyrmex that partitioning by gene, translational pattern and codon position were uniformly favoured over less Australia New Guinea complex partitions. Nuclear markers showed relatively minor sequence divergence and provided strongly New Caledonia supported topology; phylogeny based solely on mtDNA produced somewhat conflicting topology but Phylogeny offered little power to resolve species complexes. Monophyly of the genus Leptomyrmex was recovered, Divergence dating as was the sister-group relationship of ‘micro-’ and ‘macro-’ Leptomyrmex species. Divergence dating analyses estimate that Leptomyrmex arose in the Eocene (stem age 44 million years ago (ma)), and that the ‘macro-’ species diverged from the ‘micro-’ species in the early Oligocene (31 ma). Diversification of the crown group ‘macro-’ and ‘micro-’ Leptomyrmex occurred in the Miocene (15 ma and 7.9 ma, respec- tively). New Guinean and New Caledonian lineages appear to have diverged from Australian lineages only recently (4.7 ma and 10.3 ma, respectively), and the latter clade is inferred to have reached New Cale- donia from Australia via long distance dispersal. These results challenge previous hypotheses of Lepto- myrmex classification and assumptions about their historical dispersal, but are in agreement with the current knowledge of the geological history of Melanesia. Ó 2011 Elsevier Inc. All rights reserved. 1. Introduction (Moritz et al., 2000). A wealth of studies have focused on insects (Austin et al., 2004); unfortunately most of the studied taxa belong Recent studies documenting the diversification history of Aus- to widespread lineages with well-developed dispersal capabilities, tralasian and Melanesian biota have begun to illuminate temporal which blurs the signature of historical dispersal (e.g. Duffels and and spatial biogeographic patterns contributing to current mosaics Turner, 2002; Balke et al., 2007). This study reconstructs the phy- of regional and local diversity. Traditionally, occurrence patterns in logeny of a genus of ants with limited dispersal ability and with endemics lineages were attributed to Gondwanan vicariance. New a global distribution limited to Australia, New Guinea (NG) and evidence from plants, vertebrates and invertebrates points towards New Caledonia (NC) (Fig. 1): the ant genus Leptomyrmex Mayr. the importance of dispersal events in shaping distributions in Aus- Leptomyrmex is a prominent component of rain forest and wet tralasia and the western Pacific (Jønsson et al., 2010; Lucky and sclerophyll forest in Australia, New Guinea and New Caledonia. Sarnat, 2010; Keppel et al., 2009; Smith et al., 2007; Murienne These large, colorful, diurnal ants are common foragers on the et al., 2005; see also Noonan and Sites, 2010). ground and in trees in intact, mature forests (Plowman, 1981; Increasingly, divergence dating offers a temporal scale to these Wheeler, 1915), where their spider-like posture and movements evolutionary patterns, often illustrating diversifications as rela- have earned them the common name of ‘spider ants’ (Shattuck, tively recent, post-dating Gondwanan breakup (Cook and Crisp, 1999). Leptomyrmex constitutes a potentially powerful model for 2005; Crisp et al., 2004) but predating Pleistocene glaciations studies of biogeography. Most queens are wingless, thus mater- nally inherited mtDNA is expected to track local colony movement, ⇑ Present address: Department of Biology, North Carolina State University, whereas nuclear genes should reflect contributions from disper- Campus Box 7617, Raleigh, NC 27695-7617, USA. Fax: +1 919 515 5327. sive, winged males (Berghoff et al., 2008; Ross and Shoemaker, E-mail address: [email protected] 1997). As Leptomyrmex are severely dispersal-limited, colony 1055-7903/$ - see front matter Ó 2011 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2011.03.004 282 A. Lucky / Molecular Phylogenetics and Evolution 59 (2011) 281–292 Fig. 1. Global distribution of extant Leptomyrmex species, with points representing individual specimen records. Geographic ranges of the principal clades are outlined, with line weight indicating relative species diversity in each area. Regions of biogeographic importance are identified as follows: AU = Australia, BG = Burdekin Gap, CY = Cape York, MMO = McPherson–Macleay Overlap, NC = New Caledonia, NG = New Guinea. reproduction presumably involves founding queens walking to the molecular data presented here provide a robust and indepen- new nest sites (Wheeler, 1934). The exception includes several re- dent set of characters that clarify species-group and interspecific cently described and small, so-called ‘micro-’ Leptomyrmex species relationships, as well as provide a foundation for historical biogeo- (Smith and Shattuck, 2009), which possess winged queens. Deter- graphic analysis of this genus. The implications of the timeline of mining the relationship of winged to wingless Leptomyrmex is ex- divergences within this genus are discussed in relation to the bio- pected to contextualize the origin of flightlessness in this lineage. geographic context of other Australian and Melanesian endemic Despite the local abundance and visibility of these ants in areas taxa and a putative fossil of Leptomyrmex. of high conservation priority (Nakamura et al., 2007), their poten- tial to serve as habitat indicators in ecological surveys and conser- vation monitoring has not been fully realized because of difficulties 2. Materials and methods in species-level discrimination. Shattuck’s (1992) revision of the ant subfamily Dolichoderinae called attention to the need for revi- 2.1. Taxon selection sionary work in Leptomyrmex, and suggested that many of the 40 specific and subspecific designations (Bolton et al., 2007; Wheeler, Species sampling and spatial coverage spanned the diversity 1934) within the genus are likely synonymous. An extensive mor- and distribution of Leptomyrmex nearly completely. Twenty-three phological review of Leptomyrmex from major collections around of the 27 known Leptomyrmex species are represented in analyses the world overturned previously proposed species boundaries (fresh material was unavailable for one ‘macro-’ and three ‘micro-’ but found a limited number of useful characters for interspecific species: Leptomyrmex melanoticus Wheeler, Leptomyrmex aitchisoni discrimination in this genus (Lucky and Ward, 2010). This study Smith and Shattuck, Leptomyrmex pilosus Smith and Shattuck, and is the first phylogenetic analysis of the genus Leptomyrmex, and Leptomyrmex ramorniensis Smith and Shattuck), sampled from 67 A. Lucky / Molecular Phylogenetics and Evolution 59 (2011) 281–292 283 populations (Table 1). Multiple representatives of most species lated in the program MEGA4 (Tamura et al., 2007), using both were included to test species boundaries proposed by previous uncorrected p-distances and the Tamura–Nei model. morphological studies (Wheeler, 1915, 1934; Smith and Shattuck, Phylogeny was inferred using Maximum Likelihood with the 2009). Images of all ‘macro-’ Leptomyrmex species are available at program RaxML 7.0 (Stamatakis et al., 2008) and using a Bayesian the website http://www.antweb.org and in a taxonomic revision approach with the program MrBayes 3.1 (Huelsenbeck and of the genus (Lucky and Ward, 2010). Specimens were selected Ronquist, 2001), accessed through CIPRES (http://www.phylo.org). to represent the extent of species’ geographic ranges and morpho- The effect of data partitioning was investigated using both meth- logical differences, in order to accurately represent intraspecific ods, and four different partitioning strategies were employed variation. (Table 3). The first and simplest involved no partitions, the second Outgroup taxa are drawn from the closest known relatives of partitioned the data by gene, the third partitioned the data by Leptomyrmex, the dolichoderine genera Dorymyrmex Mayr and gene and by translational pattern (e.g. introns, exons), and the Forelius Emery and a distantly related dolichoderine genus, Linepit- fourth partitioned the data by all aspects: gene, translational hema Mayr (Brady et al., 2006; Ward et al., 2010). pattern, and codon position within exons (1st and 2nd position vs. 3rd position). The appropriate model of nucleotide sequence 2.2. Gene selection evolution was selected