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Multiple Convergent Evolution of Arboreal Life in Oribatid Mites Indicates the Primacy of Ecology Mark Maraun1,2,*, Georgia Erdmann3,†, Garvin Schulz1, Roy A

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Multiple Convergent Evolution of Arboreal Life in Oribatid Mites Indicates the Primacy of Ecology Mark Maraun1,2,*, Georgia Erdmann3,†, Garvin Schulz1, Roy A Downloaded from rspb.royalsocietypublishing.org on January 22, 2010 Proc. R. Soc. B (2009) 276, 3219–3227 doi:10.1098/rspb.2009.0425 Published online 17 June 2009 Multiple convergent evolution of arboreal life in oribatid mites indicates the primacy of ecology Mark Maraun1,2,*, Georgia Erdmann3,†, Garvin Schulz1, Roy A. Norton4, Stefan Scheu1,2 and Katja Domes2 1Universita¨tGo¨ttingen, Institut fu¨r Zoologie und Anthropologie, Berliner Straße 28, 37073 Go¨ttingen, Germany 2Technische Universita¨t Darmstadt, Institut fu¨r Zoologie, Schnittspahnstraße 3, 64287 Darmstadt, Germany 3Staatliches Museum fu¨r Naturkunde Go¨rlitz, Am Museum 1, 02826 Go¨rlitz, Germany 4State University of New York, College of Environmental Science and Forestry, 1 Forestry Drive, Syracuse, NY 13210, USA Frequent convergent evolution in phylogenetically unrelated taxa points to the importance of ecological factors during evolution, whereas convergent evolution in closely related taxa indicates the importance of favourable pre-existing characters (pre-adaptations). We investigated the transitions to arboreal life in ori- batid mites (Oribatida, Acari), a group of mostly soil-living arthropods. We evaluated which general force—ecological factors, historical constraints or chance—was dominant in the evolution of arboreal life in oribatid mites. A phylogenetic study of 51 oribatid mite species and four outgroup taxa, using the ribosomal 18S rDNA region, indicates that arboreal life evolved at least 15 times independently. Arboreal oribatid mite species are not randomly distributed in the phylogenetic tree, but are concentrated among strongly sclerotized, sexual and evolutionary younger taxa. They convergently evolved a capitate sensillus, an anemoreceptor that either precludes overstimulation in the exposed bark habitat or functions as a gravity receptor. Sexual reproduction and strong sclerotization were important pre-adaptations for colonizing the bark of trees that facilitated the exploitation of living resources (e.g. lichens) and served as predator defence, respectively. Overall, our results indicate that ecological factors are most important for the observed pattern of convergent evolution of arboreal life in oribatid mites, supporting an adaptationist view of evolution. Keywords: convergent evolution; adaptation; ecological niche; pre-adaptation; oribatid mites; constraints 1. INTRODUCTION 2003; Langerhans & DeWitt 2004; Zhang 2006; Marks Convergent evolution is the development of similar traits 2007). In this view, convergent evolution indicates the in different evolutionary lineages. Famous examples of limits of potential evolutionary pathways, such that differ- convergence are the similar body forms and lifestyles ent evolutionary trajectories resulted in similar solutions of marsupial and eutherian mammals, camera eyes in to the same ecological problem. For example, Morris vertebrates and cephalopods, and electrogeneration (and (2003) used convergent evolution as evidence for directed perception) in the platypus and in a number of fishes, but evolution resulting in similar endpoints, although this myriad evolutionary convergences have been discovered teleological view has been criticized (Lenski 2003). in molecules, physiological traits and complex morpho- Convergent evolution may also be a product of chance, logical adaptations (Morris 2003). The haemoglobins in as there can be more than one optimum for a trait animals, plants, protists and prokaryotes probably have (Gould & Lewontin 1979; Doolittle 1981; Gould 1989; an independent evolutionary origin (Hardison 1996), Zhang & Kumar 1997; Marks 2007). An ecological chal- echolocation call design evolved convergently in bats lenge could have been solved in a similar way by two or (Jones & Teeling 2006) and eusociality evolved conver- more species through chance alone. Further, convergent gently in insects, shrimps and mammals (O’Riain et al. evolution may result from historical contingencies of 2000). However, despite the large number of observed certain groups of organisms. Taxa may have certain pre- cases of convergent evolution, its importance and existing conditions, i.e. pre-adaptations, that result in implications are subjects of intense debate. fast radiation when environmental conditions change or For many, convergence derives from frequent and when new habitats are colonized. independent adaptations and thereby points to the impor- Oribatid mites may serve as model organisms to study tance of ecological factors during evolution (Sinclair et al. the hypothesis of the relative importance of adaptation versus chance during evolution. They are an evolutiona- rily old group that probably has existed for at least 380 *Author and address for correspondence: Universita¨t Go¨ttingen, million years (Norton et al. 1988), and they slowly but Institut fu¨r Zoologie und Anthropologie, Berliner Straße 28, 37073 continuously radiated to a large number of species; Go¨ttingen, Germany ([email protected]). †Present address: Universita¨t Go¨ttingen, Institut fu¨r Zoologie und about 10 000 species are described but overall 100 000 Anthropologie, Berliner Straße 28, 37073 Go¨ttingen, Germany. may exist (Walter & Proctor 1999; Schatz 2002). Received 13 March 2009 Accepted 27 May 2009 3219 This journal is q 2009 The Royal Society Downloaded from rspb.royalsocietypublishing.org on January 22, 2010 3220 M. Maraun et al. Convergent evolution of arboreal life Weinvestigated whether independent adaptations (caused (b) Sample preparation, PCR and sequencing by ecological factors), pre-adaptations or chance events were DNA was extracted from single individuals. Each mite was the important factors for the evolution of arboreal life in ori- placed in an Eppendorf tube, frozen in liquid nitrogen and batid mites by examining how often, and in which taxonomic crushed with a plastic rod. Total DNA was extracted using groups, arboreal lifeevolved. Oribatid mites are primarilysoil- Qiagen DNeasy Kit for animal tissues according to the man- living organisms, but numerous taxa include species with an ufacturer’s protocol (elution was performed in 30 ml instead arboreal lifestyle. Oribatid mites on trees live in particular of 400 ml; Qiagen, Germany). arboreal microhabitats such as bark or lichens, on both Amplifications were performed using the primers trunks and twigs (Proctor et al.2002; Lindo & Winchester 18Sforward (50-TACCTGGTTGATCCTGCCAG-30) and 2006; Behan-Pelletier et al.2007; Erdmann et al. 2007). 18Sreverse (50-TAATGATCCTTCCGCAGGTTCAC-30) Because arboreal oribatid mite species permanently live on (modified after Turbeville et al. 1991)in25ml volumes con- trees, they probably share morphological or behavioural taining 0.5–0.7 ml of each primer (100 pmol ml21), 5–8 ml traits (Walter & Behan-Pelletier 1999; Karasawa & Hijii DNA and 12.5 ml HotStarTaq Mastermix (1.25 U HotStar- 2004) including sexual reproduction (Behan-Pelletier & Taq polymerase, 100 mM of each dNTP and 7.5 mM Winchester 1998; Erdmann et al.2006). In contrast to oriba- MgCl2 buffer solution; Qiagen). PCR conditions were as fol- tid mites on trees, of which in temperate forests 95 per cent of lows: initial activation at 958C for 15 min, 34 amplification all individuals reproduce sexually (Erdmann et al.2006), cycles (958C for 45 s, 578C for 1 min and 728C for 1 min); parthenogenetic reproduction dominates in soil-living taxa; final elongation at 728C (10 min). in soils of temperate forests, about 80 per cent of the individ- PCR products were visualized on 1 per cent agarose gels and uals are parthenogenetic (Maraun et al.2003; Cianciolo & purified using QIAquick PCR Purification Kit (Qiagen); PCR Norton 2006; Domes et al.2007a). In soil, both oribatid products were directly sequenced by Macrogen Inc. (Seoul, mites with cuticles hardened by sclerotization or mineraliz- South Korea) using the additional primers 18S554f (50- ation and soft-bodied species coexist, whereas on trees species AAGTCTGGTGCCAGCAGCCGC-30), 18S1282r (50-TCA with soft-bodied adults are virtually absent. Soil oribatid CTCCACCAACTAAGAACGGC-30), 18S1150f (50-ATTGA mites are characterized by a large and often ornamented CGGAAGGGCACCACCAG-30) and 18S614r (50-TCCAAC sensillus, whereas in tree-living species a capitate sensillus TACGAGCTTTTTAACC-30) (modified after Turbeville et al. predominates (Aoki 1973). Further, in contrast to soil- 1991). All sequences are available at GenBank (see table 1 for living oribatid mites, many tree-living oribatid mite species accession numbers). feed on lichens (Seyd & Seaward 1984; Erdmann et al.2007). Using a large collection of oribatid mite taxa representing (c) Alignment and phylogenetic analyses most of the known tree-living taxa, we investigated how DNA sequences of the ribosomal 18S region were aligned often oribatid mites independently colonized trees. A mol- using the default settings in CLUSTALX (Thompson et al. ecular phylogeny was constructed using the ribosomal 18S 1994, 1997); the alignment was modified by eye since gaps region (18S rDNA). We also tested whether tree-living in occurred. The evolutionary model parameters were deter- oribatid mites is correlated with the traits noted above, mined with MODELTEST 3.7 (Posada & Crandall 1998) sexual reproduction, a capitate sensillus and strong scleroti- using a hierarchical likelihood ratio test. The model of evol- zation, using information from the literature (e.g. Seyd & ution was GTR þ I þ G(Tamura & Nei 1993) with base fre- Seaward 1984; Weigmann 2006; Erdmann et al. 2007; quencies A ¼ 0.2567, C ¼
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