Genetic Divergence Between the Sympatric Queen Morphs of the Ant Myrmica Rubra

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Genetic Divergence Between the Sympatric Queen Morphs of the Ant Myrmica Rubra Molecular Ecology (2015) 24, 2463–2476 doi: 10.1111/mec.13170 Genetic divergence between the sympatric queen morphs of the ant Myrmica rubra € € € € JENNI LEPPANEN,* PERTTU SEPPA,† KARI VEPSALAINEN* and RIITTA SAVOLAINEN* *Department of Biosciences, University of Helsinki, P.O. Box 65, Helsinki 00014, Finland, †Centre of Excellence in Biological Interactions, Department of Biosciences, University of Helsinki, P.O. Box 65, Helsinki 00014, Finland Abstract Pairs of obligate social parasites and their hosts, where some of the parasites have recently diverged from their host through intraspecific social parasitism, provide intriguing systems for studying the modes and processes of speciation. Such specia- tion, probably in sympatry, has also been propounded in the ant Myrmica rubra and its intraspecific social parasite. In this species, parasitism is associated with queen size dimorphism, and the small microgyne has become a social parasite of the large macro- gyne. Here, we investigated the genetic divergence of the host and the parasite queen morphs in 11 localities in southern Finland, using nuclear and mitochondrial markers of queens and workers. We formulated and tested four speciation-related hypotheses that differed in the degree of genetic divergence between the morphs. The queen mor- phs were genetically distinct from each other with little hybridization. In the nuclear data, when localities were nested within queen morphs in the hierarchical AMOVA, 39% F’ = of the genetic variation was explained by the queen morph (standardized CT 0.63, F = F’ = uncorrected CT 0.39), whereas 18% was explained by the locality ( SC 0.39, F = hypothesis of advanced sympatric speciation SC 0.29). This result corroborated the . In contrast, the mitochondrial DNA could not settle between the hierarchical levels of locality and queen morph, thus substantiating equally the hypotheses of incipient and advanced sympatric speciation. Together, our results support the view that the microgy- nous parasite has genetically diverged from its macrogynous host to the level of a nas- cent species. Keywords: hymenoptera, inquilinism, Myrmica microrubra, size dimorphism, social parasitism, sympatric speciation Received 29 July 2014; revision received 18 March 2015; accepted 19 March 2015 Promising candidates of sympatric speciation are Introduction found in some obligate social parasites of ants (Was- One of the most debated evolutionary questions dur- mann 1909; Elmes 1978; Buschinger 1990; Bourke & ing the last decades has focussed on the modes of Franks 1991; Mayr 1993). According to Emery’s rule, speciation, particularly on speciation in sympatry (Fitz- social parasites are closely related to their host (Le Mas- patrick et al. 2009). Nowadays, it is widely accepted ne 1956), which has been shown in many obligate social that sympatric speciation occurs (Via 2001), but most parasites (Huang & Dornhaus 2008; Buschinger 2009; examples have been criticized as they rarely fulfil all and references therein; Jansen et al. 2010). This has the criteria for sympatric speciation (reviewed by Fitz- prompted the hypothesis that some social parasites patrick et al. 2009). The prevalence of sympatric specia- have evolved from their hosts sympatrically through tion is unclear but probably rare (Fitzpatrick et al. intraspecific social parasitism (Elmes 1978; Buschinger 2009). 1990; Bourke & Franks 1991). Speciation in sympatry is often, however, difficult to distinguish from the alterna- tive scenario, speciation in allopatry followed by symp- Correspondence: Jenni Leppanen,€ Fax: +358 294157692; E-mail: jenni.leppanen@helsinki.fi atry (Smith et al. 2007). Therefore, it would be ideal to © 2015 John Wiley & Sons Ltd € 2464 J. LEPPANEN ET AL. study speciation when it is still an ongoing process and other. Both locality and morph levels explain significant allopatry can be ruled out. amounts of the genetic variation in the system, but the The ant genus Myrmica has many social parasites locality level explains a larger proportion than the (Radchenko & Elmes 2003) that are closely related to morph level. (iii) The hypothesis of advanced sympatric their hosts (Savolainen & Vepsal€ ainen€ 2003; Jansen et al. speciation claims that the two morphs have diverged 2010). One of these host–parasite pairs is M. rubra and from each other clearly. Both locality and morph levels its queen morphs, which are easily distinguished from explain significant amounts of the genetic variation in each other by size (Seifert 1993). The microgynes usu- the system, but the morph level explains a larger pro- ally produce no or only a few workers (Elmes 1976); portion than the locality level. (iv) According to the such social parasites are called inquilines (Wilson 1971). two-species hypothesis, the two morphs have fully Because inquilines lack a functional worker caste, they diverged from each other and can be considered as sep- are totally dependent on their macrogynous host. Con- arate species. In this case, the locality level explains sequently, in spite of a vast body of work on M. rubra’s only a minor part of the genetic variation in the system, microgyne, no documented observation on its reproduc- depending on the spatial structure and gene flow in the tion is known outside colonies of the host. In parasit- two species in question. We argue that in the second ized nests, which often form large polydomous colonies and third hypotheses, speciation is sympatric, as the mi- (supercolonies; Seppa€ & Pamilo 1995; Walin et al. 2001), crogynous morph is dependent on its macrogynous breeding queens of both morphs typically are present host, and the locality explains a significant amount of in large numbers (Elmes 1976; Seppa€ & Walin 1996). genetic variation. In the fourth hypothesis, the specia- When the microgynous parasite is present in a nest, it tion mode (allopatry vs. sympatry) is, however, less produces an excessive amount of sexual offspring (Pear- clear as speciation is already complete. son 1981) and can suppress the growth of sexual off- spring of the macrogynes, which supply the workers Materials and methods (Elmes 1976; Pearson 1981). Because each queen morph produces only offspring of its own kind, queen size is Sampling presumably genetically regulated (Elmes 1976; Seifert 2010). We collected 80 nest samples of Myrmica rubra from 11 The taxonomic status of the microgynous morph has localities in southern Finland (Fig. 1, Table 1). We been debated and alternated over the past decades. Seif- selected nests at least three metres apart from each ert (1993) described the microgynous morph as a new other and sampled workers and all micro- and macrog- species, M. microrubra, but later it was synonymized ynous queens that we found and preserved them in with M. rubra (Steiner et al. 2006). Nevertheless, the absolute ethyl alcohol. The queens were separated by documented genetic differentiation between the queen visual inspection into either queen morph; no interme- morphs (Pearson & Child 1980; Pearson 1981; Steiner diate individuals were found. All macrogynes were et al. 2006; Vepsal€ ainen€ et al. 2009; Leppanen€ et al. 2011; wingless, presumably established queens, except for Schar€ & Nash 2014) may owe to ongoing speciation (Sa- one winged gyne from each of three nests. The mi- volainen & Vepsal€ ainen€ 2003; Seifert 2007, 2010; crogynes included both wingless, presumably old Vepsal€ ainen€ et al. 2009). To evaluate the postulated spe- queens, and winged gynes. ciation, however, more data on the genetic differentia- For nuclear DNA genetic analyses, we generally used tion between the two morphs are needed. eight macrogynes and eight microgynes from each nest. Here, we studied the genetic composition and spatial As eight macrogynes were not available in all nests, we structure of M. rubra in multiple localities where the mi- supplemented the data by analysing up to eight workers crogynous and macrogynous morphs (the parasite and from these nests. Altogether, our data consisted of 511 the host) co-occur. By investigating the genetic diver- microgynes, 136 macrogynes and 500 workers (Table 1). gence between the locally co-occurring (syntopic, living We used 40 earlier published COI and cyt b mito- side by side) morphs and among the localities of each chondrial DNA sequences (Savolainen & Vepsal€ ainen€ morph, we tested the following four speciation-related 2003; Vepsal€ ainen€ et al. 2009; Leppanen€ et al. 2011) from hypotheses that are based on the hierarchical distribu- eight localities where we also had nuclear data (Table tion of genetic variation at locality and morph levels. (i) S1, Supporting information). The mitochondrial According to the single-species hypothesis, the two mor- sequences included 18 microgynes and four macrogy- phs have not diverged from each other, and the morph nes, but as the Bayesian clustering of nuclear data veri- level explains poorly the genetic variation in the system. fied that most workers were produced by the (ii) The hypothesis of incipient sympatric speciation states macrogynes, 18 workers were used to represent macro- that the two morphs have started to diverge from each gynes when queens were not available. © 2015 John Wiley & Sons Ltd GENETIC DIVERGENCE OF SYMPATRIC ANT QUEEN MORPHS 2465 Fig. 1 Sampling areas in southern Fin- land; the area numbers refer to (1) 100 km Tvarminne,€ localities TK and TN; (2) Karjaa, KA; (3) Vermo, VE; (4) Pikku- Huopalahti, PH; (5) Viikki, VF, VL, VM and VP; (6) Uutela, UU; and (7) Sipoo, SI. For locality information, see Table
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