Eusociality and the success of the termites ... - Wiley Online Library

doi: 10.1111/j.1420-9101.2009.01789.x

Eusociality and the success of the termites: insights from a supertree of dictyopteran families R. B. DAVIS, S. L. BALDAUF 1 & P. J. MAYHEW Department of Biology, University of York, York, YO10 5YW, UK

Keywords:

Abstract

Ancestral states; Dictyoptera; eusociality; extinction; Isoptera; macroevolution; phylogeny; speciation; species richness; supertree.

Sociality in insects may negatively impact on species richness. We tested whether termites have experienced shifts in diversification rates through time. Supertree methods were used to synthesize family-level relationships within termites, cockroaches and mantids. A deep positive shift in diversification rate is found within termites, but not in the cockroaches from which they evolved. The shift is responsible for most of their extant species richness suggesting that eusociality is not necessarily detrimental to species richness, and may sometimes have a positive effect. Mechanistic studies of speciation and extinction in eusocial insects are advocated.

Introduction Eusociality has long fascinated evolutionary biologists. It has evolved a rather limited number of times and poses an obvious challenge; namely to explain its origins and maintenance through Darwinian processes (Darwin, 1859; Hamilton, 1964; Andersson, 1984; Smith & Szathma´ry, 1995; Wilson, 2008). Although substantial research into eusocial insects focuses on the causes of eusociality, eusociality also has interesting potential evolutionary consequences. One such consequence is the evolution of social interactions between colonymembers (Trivers & Hare, 1976; Ratnieks & Visscher, 1989), and another is the subsequent evolution of interspecific interactions, such as parasitism and mutualism (Schmidt-Hempel, 1998; Aanen et al., 2002). Another is the effects of eusociality on species richness through its effects on speciation and extinction rates. In this paper, we address changes in these rates over time in one of the major groups of eusocial insects, the termites (Isoptera). Although the evolution of eusociality has long been regarded, in a general sense, as a significant step in insect evolution (Carpenter, 1992), the macro-evolutionary consequences of eusociality have been little studied. Correspondence: Robert B. Davis, Department of Biology, University of York, York, YO10 5YW, UK. Tel.: 01904 328633; e-mail: [email protected] 1 Current address: Department of Evolutionary Biology, Uppsala University, Uppsala, Sweden.

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Wilson (1992) suggested that, in contrast to social vertebrates, social invertebrates have slower rates of evolution and are characterized by relatively low diversity compared with nonsocial forms. The reason suggested is that social insects effectively act like ecological superorganisms, giving them a low carrying capacity at the level of the colony, and lower effective population sizes. Indeed conservation studies suggest that this has been important in recent declines of several eusocial species (Chapman & Bourke, 2001; Darvill et al., 2006; Ellis et al., 2006), and some fossil studies also suggest that some groups of eusocial insects have suffered high extinction rates contributing to low net rates of diversification (Engel, 2001). In contrast to these extinction studies, however, some phylogenetic studies (Moreau et al., 2006) suggest considerable adaptive radiation into new niches in eusocial groups suggesting that eusociality can also provide opportunities for evolutionary diversification. Furthermore, some molecular evidence suggests increased, rather than decreased rates of molecular evolution in eusocial insects (Luchetti et al., 2005). Thus, formal macro-evolutionary studies are required within a range of eusocial insect groups to fully understand the role that eusociality may play. The termites (Isoptera) are a widespread group of social insects that play an important ecological role through their effects on wood and litter decomposition in tropical and subtropical environments (Eggleton et al., 1996; Ohkuma, 2003; Apolina´rio & Martius, 2004). Unlike bees, wasps and ants, termites are diplodiploid and much

ª 2009 THE AUTHORS. J. EVOL. BIOL. 22 (2009) 1750–1761 JOURNAL COMPILATION ª 2009 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY

Dictyoptera evolution

attention has been paid to how eusociality can have originated and be maintained, in the absence of the inclusive fitness benefits resulting from haplodiploidy (Thorne, 1997; Thorne et al., 2003; Wilson & Holldo¨bler, 2005). Termites also engage in a number of mutualistic symbioses with other species, themselves a challenge to evolutionary biology (Aanen et al., 2002; Ohkuma, 2003; Mayhew, 2006). Phylogenetic studies at the level of the order (Mayhew, 2002, 2003) do not suggest that Isoptera have experienced a large or significant shift in diversification, but those studies assumed monophyletic orders (see below), and conclusions are sensitive to other phylogenetic assumptions (Mayhew, 2003). Fossil evidence for termites suggests that the currently rather species poor and restricted primitive families (e.g. Mastotermitidae, Hodotermitidae and Termopsidae) were once more diverse and widely distributed. The most species-rich family, the Termitidae, is derived phylogenetically and also has a more recent fossil record. Overall this suggests that changes in diversification, including perhaps extensive past extinction and more recent radiation, have occurred (Thorne et al., 2000; Grimaldi & Engel, 2005). However, there have been no formal macro-evolutionary tests that incorporate family-level phylogenetic information. The incidence and timing of shifts in net diversification within the termites therefore remains unclear. A critical understanding of phylogeny is essential to locating shifts in diversification rates (Purvis, 1996). Together with the orders Mantodea (mantids) and Blattaria (roaches), the order Isoptera comprises the Dictyoptera. The monophyly of the Dictyoptera is arguably one of the least controversial aspects of insect phylogeny (Hennig, 1981; Kristensen, 1981; Wheeler et al., 2001), but the interrelationships of these orders has been debated (Thorne & Carpenter, 1992; Klass & Meier, 2006). Current opinion supports a Blattaria–Isoptera clade to which Mantodea are sister (Klass & Meier, 2006). At family-level, blattarian–isopteran relationships have received much attention particularly the position of Cryptocercidae in relation to the Isoptera, and the suggestion that Blattaria may in fact be paraphyletic to Isoptera (Klass & Meier, 2006; Inward et al., 2007a; Ware et al., 2008). There have been various morphological (Donovan et al., 2000; Klass & Meier, 2006) and molecular (Kambhampati, 1995, 1996; Kambhampati & Eggleton, 2000; Thompson et al., 2000; Inward et al., 2007a) studies conducted for these two traditional orders, and while some relationships are more well established (e.g. Blaberidae + Blattellidae), other families (e.g. Termopsidae) are harder to place. Figure 1 shows some previous family-level phylogenies of the Isoptera. Eggleton (2001) has suggested an all-inclusive analysis would be useful in elucidating termite family relationships. In contrast, mantodean family relationships are far less studied (Grimaldi, 2003; Svenson & Whiting, 2004), and lack of

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(a)

(b)

(c)

Fig. 1 Previous phylogentic hypotheses of Isoptera recognizing the seven families considered in this study. (a) Donovan et al. (2000), (b) Kambhampati & Eggleton (2000) and (c) Thompson et al. (2000).

consensus on a family-level taxonomy has perhaps hindered progress here (Svenson & Whiting, 2004). In this paper, we first use supertree techniques (Bininda-Emonds, 2004a,b) to assess the family-level relationships of Dictyoptera, synthesizing the evidence from previously published analyses. We ask if the phylogenetic relationships imply shifts in diversification within the termites. We then investigate changes in key ecological and behavioural traits, as potential key innovations that might explain any diversification shifts.

Materials and methods Taxonomic nomenclature The taxonomic nomenclature is taken from a family list generated from Gordh & Headrick (2000) for living


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families and Ross & Jarzembowski (1993) and the regularly updated EDNA Fossil Insect Database (http:// edna.palass-hosting.org/search.php) for extinct families. Taxa not recognized on this list were not considered in the supertree analysis. Input trees A total of 26 input trees formed the final data set. For search criteria see Appendix S1 in Supporting Information. Within these trees valid taxa (see taxonomic nomenclature) were sometimes either paraphyletic or polyphyletic, for example in molecular data sets where families were split across several species. In these instances, polyphyletic families were removed entirely as their placement is uncertain. Paraphyletic families were condensed into a single branch. This was essential as distance-based methods are unable to cope with paraphyletic or polyphyletic taxa. Supertree methods Many previous supertree studies (Purvis, 1995a; BinindaEmonds et al., 1999; Jones et al., 2002; Pisani et al., 2002; Salamin et al., 2002; Ruta et al., 2003; Davies et al., 2004; Grotkopp et al., 2004; Beck et al., 2006; Cavalcanti, 2007) have used the popular matrix representation with parsimony (MRP) method (Baum, 1992; Ragan, 1992) only, but we implement six supertree methods; four matrixbased and two-distance-based, to avoid over-reliance on a single method. In addition to MRP, we use Purvis MRP (Purvis, 1995b), matrix representation with compatibility (Ross & Rodrigo, 2004), matrix representation with flipping (Eulenstein et al., 2004), the average consensus method (Lapointe & Cucumel, 1997) and the most similar supertree method or distance fit (dfit) method (Creevey et al., 2004). We avoided using agreement supertree methods as they only identify relationships common to all input trees. For software and settings see Appendix S2. Data non-independence is a major problem with supertree analyses, but following the guidelines of Bininda-Emonds et al. (2004), we ensure data nonindependence between all contributing input trees is minimized (see Appendix S1). We use the V Index of Wilkinson et al. (2005) to measure support. This considers the number of input trees in agreement and in conflict with relationships in the supertree. Dating the supertree The preferred supertree was dated using two techniques, providing respectively conservative and liberal dates, so that sensitivity of evolutionary inferences could be tested. Minimum first appearances were used to provide conservative hard evidence dates for the origin of families (Ross & Jarzembowski, 1993; Mitchell, 2007).

In addition to this, where the supertree corresponded to a molecular phylogeny, theoretical maximum dates were placed on nodes. The program r8s (Sanderson, 2003) was used to make the molecular tree ultrametric (see below) and the method of Marshall (2008) employed to obtain maximum dates, whereby the taxon with the most complete fossil record, as measured by an empirical scaling factor (see Results), is used to calibrate the tree and confidence intervals on those dates are assigned using the completeness of the record of other taxa. For details of dating methods see Appendix S2. Diversification analysis Two tests using contrasting information and assumptions, also employed by Mayhew (2002) in an insect order-level diversification analysis, were used to assess whether any significant shifts in diversification have occurred during the evolution of the Blattaria and Isoptera. The first assesses where there is a significant difference in sister taxon species richness. Care must be taken when interpreting the results of this analysis, as a seemingly significant difference in species richness at a more basal node may be attributable to such an occurrence towards the crown (i.e. a ‘trickle-down’ effect). We therefore use the method of Davies et al. (2004) to account for this (see also Hunt et al. 2007). Such procedures have proved reasonably effective at eliminating trickling down problems in simulations (Moore et al., 2004). The second test calculates the mean radiation rate for each family. Confidence intervals can be placed on these estimates (Purvis, 1996) to allow comparison across all terminal taxa and assess which families have diversified more rapidly. In contrast to the first test, this test uses date information but simpler assumptions regarding evolution. We also applied this test to sister taxa, and accounted for the trickle-down effect in the same manner as for the first test. For details of tests see Appendix S2. To conduct both tests species numbers for all families must be known. For Isoptera these figures were taken from (Grimaldi & Engel, 2005) and for Blattaria these were taken from the Blattodea Species File Online created by George Beccaloni (NHM, London) at http:// blattodea.speciesfile.org, which contains records of all living roach species as recently as 2007. These numbers are described species only, and while these will likely be underestimates of total species numbers, the first diversification test is robust to underestimation of species richness as long as it is unbiased across taxa (Nee et al., 1994). Ancestral states and trait mapping in Isoptera Here we take the likelihood approach to reconstructing ancestral character states. By using the likelihood



approach we remove ourselves from previous debates on the correct use of parsimony reconstructions (Thompson et al., 2000, 2004; Grandcolas & D’Haese, 2002, 2004). Additionally, we are able to use branch length information (i.e. time), and our results are based on explicit models of evolution, which can be assigned probabilities, which aids interpretation. Robustly determined ancestral states coinciding with a shift in diversification represent potential explanatory key innovations (Mayhew, 2002). Analysis was carried out using BayesTraits (Pagel et al., 2004) using the ‘Multistate’ mode and maximum likelihood algorithm, using either a one- or two-rate model as appropriate (for details of method see Appendix S2). The five traits studied in this analysis come from Higashi et al. (2000) and are presented in Table 1, and represent behavioural and ecological traits that could potentially affect macroevolution. The presence or absence of a true, sterile worker caste, refers to individuals which have developed irreversibly and perform helper tasks in colonies. Some families instead have individuals that can reverse back from a worker state and are therefore not considered true workers (Roisin, 2000). With the same pattern of distribution across families is termite foraging strategy (or ‘life type’ of Higashi et al.), which is either one-piece (i.e. foraging in the place they nest), or separate (or intermediate, grouped here together as in Thompson et al. (2000)), which involves foraging at distant foraging sites (Thompson et al. (2000). The other traits examined are diet, nest type and colony size. All traits are treated as discrete including colony size where only two sizes (104 and 106) are given by Higashi et al. (2000); there is no evidence that intermediate colony sizes exist in any terminal taxa. Only where we have relevant information on the outgroup to Isoptera do we include it in these analyses. Table 1 Traits examined here taken from Higashi et al. (2000) [Source: Serritermitidae taken from Thompson et al. (2000)].

Family

Worker

Foraging strategy

Cryptocercidae Mastotermitidae Hodotermitidae Termopsidae Kalotermitidae Serritermitidae Rhinotermitidae Termitidae

N⁄A T T F F T T T

N⁄A S S O O S S S

Food

Nest

W W DG W W ? W W ⁄ DG ⁄ DL ⁄ S ⁄ Li

W W⁄S S W W ? W⁄S W⁄S⁄ E⁄A

Colony size N⁄A 104 ? 104 106 ? 106 106

Worker: T, true (sterile); F, false; Foraging strategy: S, separate or intermediate; O, one-piece; Food: W, wood; DG, dead grass; DL, dead leaves; S, soil; Li, lichen; Nest: W, wood; S, subterranean; E, epigeal; A, arboreal. Also included are character states (where applicable) for the termite sister taxon Cryptocercidae.

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Results Dictyopteran phylogeny Inclusion of fossil taxa from the Grimaldi (2003) input tree (the only input tree containing fossil taxa) produces a standard MRP supertree in which only the Mantodea are resolved (not shown). Rerunning the analysis omitting these fossil families results in six equally optimal trees in which blattarian–isopteran relationships are identical. Regarding key relationships, Mantodea are sister to a Blattaria–Isoptera clade and the blattarian family Cryptocercidae are sister to Isoptera making ‘Blattaria’ paraphyletic. Regarding mantodean relationships there is a basal polytomy in the strict consensus of these equally optimal trees consisting of Chaeteessidae, Mantoididae and a clade of the other families. Before fossil taxa were removed Chaeteessidae was sister to all other mantids. There is also another polytomy between Amorphoscelidae, Eremiaphilidae and a clade of three mantid families. Even in a majority-rule consensus these are not resolved as the alternative relationships appear in equal numbers across the most parsimonious trees (MPTs). The three other matrix-based supertree methods all produce the same set of equally optimal trees. All relationships are well supported as indicated by positive V Scores and an overall supertree V Score of +0.733, indicating a large agreement regarding relationships in dictyopteran phylogenies to date. This preferred tree is shown in Fig. 2. The distance-based methods also produce supertrees in which Mantodea (or at least representatives of Mantodea) are sister to a Blattaria–Isoptera clade. In this clade, the relationships are identical to those produced by the matrix-based supertree methods. Mantodean relationships differ in both average consensus and dfit supertrees. The average consensus method produces a supertree, which positions the mantodean family Empusidae as sister to the Blattaria–Isoptera clade, with the rest of Mantodea forming a separate clade. Interestingly Amorphoscelidae and Eremiaphilidae, the positions of which cannot be resolved using matrix-based methods, are represented as sister families here (Fig. 2). This supertree obtains a lower V Score of +0.460. The dfit analysis produces three equally optimal trees, the strict consensus of which shows Mantoididae sister to all other mantids. Chaeteessidae is the next family to branch off before a five-way polytomy of six families in which only Empusidae and Hymenopodidae are shown to be sister taxa. To obtain a fully bifurcating topology a 50% majority rule tree with minority components was made. From this previous polytomy Metallyticidae falls out as sister to two other small clades. One consists of Mantidae, Empusidae and Hymenopodidae as in the matrix-based supertrees and the other contains Amorphoscelidae and Eremiaphilidae (Fig. 2). This supertree obtains a high V Score of +0.731.


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Fig. 2 A supertree of dictyopteran families. Unbroken lines represent the preferred phylogeny recovered using all matrix-based supertree methods. Dashed lines indicate alternative relationships recovered using distance-based methods. Numbers on nodes indicate support according to the V Index. Numbers associated with blattarian and isopteran families indicate taxon species richness. Open stars indicate where a positive shift in diversification has been detected using one of the two tests, and shaded stars indicate where a negative shift in diversification has been detected.

Conservative and liberal branching dates With ghost ranges inferred, we conservatively estimate the minimum first appearance date of the lineage that gave rise to crown Dictyoptera at 203.5 Mya [i.e. the minimum first appearance date of Blattulidae; the fossil roachoid sister group to modern Dictyoptera according to Grimaldi & Engel (2005)] in the early Jurassic. We estimate the origin of Mantodea to be around 141 Mya in the early Cretaceous, and the origin of the ‘Blattaria’ + Isoptera at 163.3 Mya in the mid-Jurassic. The Isoptera alone, are estimated to originate around the same time as the Mantodea. For a complete list of fossil dates, see Appendix S3. As the topology for Isoptera in the supertree matches the molecular tree of Thompson et al. (2000), built using large subunit rRNA and cytochrome oxidase II genes, we produce a molecular dated tree for this order. The tree was calibrated using the maximum date for Rhinotermitidae (88.5 Mya) as this has the largest scaling factor (see Appendix S2). Although we have less temporal resolution for this family than the others (epoch rather than stage), this date is statistically not an outlier when compared with the dates of other families and is therefore acceptable to use (Kolmogorov-Smirnov test, P = 0.945, see Marshall, 2008). Despite the earliest termite fossil being from the Cretaceous, the method does suggest that the Isoptera may have split from

Blattaria at least as early as the Carboniferous (291.24 Mya), and the first split within Isoptera leading to modern families (i.e. Mastotermitidae) in the Triassic (227.11 Mya) (Fig. 3). With 95% confidence intervals added for an absolute maximum (Fig. 3), the date for the split of Isoptera within ‘Blattaria’ is unacceptably old (479.84 Mya; Ordovician) before hexapods as a whole are believed to have originated. This is partly a result of having rather few terminal taxa with a fossil record leading to large confidence intervals. Also the confidence intervals are inherently generous in the absence of quantitative on the fossil distributions of each family (Marshall, 2008). Diversification Herein, we focus on the evolution of ‘Blattaria’ and Isoptera, using the fully bifurcating topology of these two orders that is recovered consistently by supertree analysis, with alternative topologies considered below. Using the first test comparing sister group species richness, significant differences in diversification are detected between Hodotermitidae + Termopsidae and Kalotermitidae + Serritermitidae + Rhinotermitidae + Termitidae and between Serritermitidae and Rhinotermitidae + Termitidae. The Kalotermitidae + Serritermitidae + Rhinotermitidae + Termitidae lineage represents a positive shift in diversification, while the Serritermitidae lineage alone



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Fig. 3 The supertree topology for Isoptera dated based on the molecular data of Thompson et al. (2000), and calibrated according to the maximum first appearance date of Rhinotermitidae. The geological time scales represent the dates given with or without a +95% confidence interval placed on the date for Rhinotermitidae. For the geological time scales O, Ordovician; S, Silurian; D, Devonian; C, Carboniferous; P, Permian; Tr, Triassic; J, Jurassic; K, Cretaceous; T, Tertiary. Thick lines on branches represent the extent of the fossil record for each family relating to the geological time scales without the 95% confidence interval. Thick lines below branches represent the extent of the fossil record if the 95% confidence interval is considered.

represents a negative shift (Table 2, see Appendix S4 for sister group species richness data). Comparing mean radiation rates under the pure birth model indicates that the Termitidae have exhibited the most rapid radiation rate of any family, although this is not significantly different from a few other rapidly radiating families; Blaberidae, Blattellidae, Kalotermitidae, Rhinotermitidae. The two more inclusive clades which have experienced comparable rapid radiations are the Termitidae + Rhinotermitidae and this clade plus Serritermitidae. The monotypic families Serritermitidae and Mastotermitidae exhibit the lowest mean radiation rates. Testing mean radiation rates accounting for trickledown in a phylogenetic context, a positive shift in radiation rate is detected along the branch representing Isoptera to the exclusion of Mastotermitidae (Table 2). A significant difference between the clade comprising Isoptera + Cryptocercidae and the Blattidae is also noted but neither a positive shift in the Blattidae or negative shift in the Isoptera + Cryptocercidae is detected when compared with the outgroup (i.e. all other blattarian families) (see Supporting Information S1 for mean radiation rates).

These results are unaffected by using either minimum or maximum dates for nodes within Isoptera, although mean radiation rates are overall lower given older dates based on molecular estimates. Species richness comparisons using the topology of Donovan et al. (2000) (the majority rule consensus of the three hypotheses shown in Fig. 1 (Eggleton, 2001) also show a negative shift in the Serritermitidae and a positive shift in the clade Table 2 Shifts in diversification within the Dictyoptera. Clade

Potential shift

Test

Mastotermitidae vs. other Isoptera Hodotermitidae + Termopsidae vs. Kalotermitidae + Serritermitidae + Rhinotermitidae + Termitidae Serritermitidae vs. Rhinotermitidae + Termitidae

(+) Other Isoptera

Pure birth rate comparisons Sister-richness comparisons


(+) Kalotermitidae + Serritermitidae + Rhinotermitidae + Termitidae

()) Serritermitidae

Sister-richness comparisons

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comprising the Kalotermitidae, Serritermitidae, Rhinotermitidae and Termitidae. The phylogeny of Kambhampati and Eggleton does not recognize this clade, and actually shows only an alternative positive shift in the Rhinotermitidae and Termitidae. See Supporting Information S1 for details of analysis. Potential key innovations For these analyses, we take Cryptocercidae as the outgroup to Isoptera as confirmed by supertree analyses, but as we only have information on their diet and nest type (other traits are not relevant to Cryptocercidae) we only include them in analyses of those traits. The maximum likelihood approach yielded no significant findings regarding the probability of ancestral states of the traits presented by Higashi et al. (2000) at internal nodes given either a tree dated using the fossil record or using molecular estimates, and referring to the most appropriate model of evolution (i.e. one or two-rate model). Individual traits are discussed below regarding the probabilities alone. Firstly, the presence or absence of the true worker caste (and of the separate foraging strategy), which has been the focus of other studies, has roughly equal probabilities at most internal nodes. The probability swings towards an ancestral true worker in the common ancestor to Serritermitidae, Rhinotermitidae and Termitidae, and in the common ancestor to Rhinotermitidae and Termitidae (Fig. 4). The one-rate model is most appropriate for analysing the evolution of this trait as both models provide similar likelihood scores (see Appendix S5). Regarding diet, at all internal nodes each possible ancestral state has a probability close to 0.2 using fossil dates, and exactly 0.2 given molecular dates when the two-rate model is used. The one-rate model provides significant results in favour of a wood feeding ancestor at all internal nodes given fossil dates, but the likelihood score is significantly different between one and two-rate models (see Appendix S5) so we must consider the tworate model here. For the tree dated with fossils, the highest probabilities are seen at the node including Kalotermitidae, Serritermitidae, Rhinotermitidae and Termitidae and the two nodes nested within, which are marginally in favour of a wood feeding ancestor, with a probability of around 0.22. Regarding nest type all possible ancestral states have exactly the same probability (0.25) of occurring at each internal node using the two-rate model. The one-rate model provides significant results in favour of a wood nesting ancestor at all internal nodes given either fossil or molecular dates, but the likelihood score is significantly different between one and two-rate models (see Appendix S5) so we must consider the two-rate model here. Regarding colony size, only at the deepest node in the tree (including all Isoptera) are the probabilities roughly even. The probability is more obviously in favour of a

Fig. 4 The supertree topology for Isoptera with ancestral trait probabilities for true or false worker and colony size based on the nonrestricted model of evolution. Sets of four pie charts show: top left – true or false worker probabilities calculated using fossil dates; top right – true or false worker probabilities calculated using molecular dates; bottom left – colony size probabilities calculated using fossil dates; bottom right – colony size probabilities calculated using molecular dates. Lifestyle probabilities are equivalent to worker probabilities (see supplementary Material S1). Circles associated with taxon names show trait states of terminal taxa (top, worker ⁄ lifestyle; bottom, colony size). Nest type probabilities are all equal (0.25), and diet probabilities are all approximately equal (0.2) and are not displayed.

small colony size at the nodes including all Isoptera to the exclusion of Mastotermitidae and at the node including just Hodotermitidae and Termopsidae. At the node including Kalotermitidae, Serritermitidae, Rhinotermitidae and Termitidae, there is a shift towards a larger colony size being the more probable ancestral state (in excess of 0.91 here using fossil dates and at more exclusive nodes within – Fig. 4). Despite this, likelihood scores still show this to be nonsignificant. The one-rate



model is most appropriate for analysing the evolution of this trait as both models provide similar overall likelihood scores (see Appendix S5). For all probabilities and likelihood scores see Appendix S5.

Discussion The most important finding of this study is that there has been a significant increase in diversification deep within termite phylogeny, with potential implications for the evolutionary consequences of eusociality. This finding is robust to alternative topologies and dates. There is a strong consensus in many areas of the phylogeny of Dictyoptera families, but with Mantodea relationships as a particular opportunity for further work. An unexpected finding was that crown termites may have originated much earlier than the hard fossil evidence suggests. Ancestral state reconstruction for key ecological and behavioural traits remains problematic at family level. Below we discuss each of these issues in greater depth. Diversification shifts Our analyses confirm, robustly, that an increase in net diversification rate has occurred deep in the termite phylogeny. The species richness of the clades above the shift, wherever it occurred, is many times that of the clades below the shift, suggesting that it has been responsible for the majority of the current richness of the order. However, the precise location of the shift depends on the underlying analysis. Furthermore, none of these potential shifts is actually at the origin of the Isoptera suggesting that if eusociality is causally linked to the shift, it is contingent on other characteristics or events, something that is likely to be common with key innovations (de Queiroz, 2002). Progress in narrowing down the location is only likely to come with greater understanding of the true underlying evolutionary processes (e.g. relative levels of speciation and extinction, constant or variable rates) so that these can be incorporated into statistical tests. Ultimately, this will probably require more detailed phylogenetic information (i.e. within families). The first possible shift, detected by comparions of radiation rates under a pure birth model, concerns the positive radiation of the Isoptera to the exclusion of Mastotermitidae, and may be attributable to a whole host of ‘more termite-like’ characters appearing along this branch of the tree. It is important to acknowledge the fossil record of Mastotermitidae, which once had a global distribution and is now a relict family with just one surviving member (Emerson, 1955; Thorne et al., 2000). Although the net rate of diversification of this family has been low overall, the fossil record might imply that it was higher in the past. Clearly, no amount of phylogenetic information that is restricted to one extant species is going to detect such shifts and a combination of detailed

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fossil and phylogenetic information that included extinct species would be necessary. The next shift detected up the tree (using sister-richness comparisons) shows a significant positive shift in diversification in the branch to the Kalotermitidae, Serritermitidae, Rhinotermitidae and Termitidae. The size of the average colony of these families is 106 compared with 104 in other families (Higashi et al., 2000). This increase in colony size could be linked to a positive shift in diversification, and it could be argued that such an increase in colony size could give them some kind of competitive edge (e.g. increased foraging), but as shown by maximum likelihood ancestral trait mapping it is not certain that the common ancestor to these families had a large colony size, despite the probability of this being high. A negative shift represented by the family Serritermitidae might be explained by considering the specialized lifestyle of its sole representative Serritermes serrifer. It lives in the outer walls of Cornitermes (Termitidae) nests, where it excavates galleries rather than building a nest of its own (Araujo, 1970). This is arguably a fairly specialist niche, which could give them a reduced potential to diversify (Kassen, 2002). A conversion to such a specialist lifestyle may have had an impact on their average colony size but this is following the shift associated with an increase in colony size, and does not influence earlier findings. Furthermore, the mandibles of S. serrifer are unique in their morphology in both the imago-worker and soldier castes compared with other species (Araujo, 1970; Krishna, 1970; Emerson & Krishna, 1975). With the discussion of a possible negative shift in the Serritermitidae branch of the isopteran tree it is pertinent to discuss the validity of this family, which has had a fairly chequered history. S. serrifer was first placed in its own family by Emerson (1965) after being variously placed in the Kalotermitidae, Rhinotermitidae or Termitidae (Emerson & Krishna, 1975; Richards & Davies, 1977). Had S. serrifer still been a member of the one of these larger families, any such negative shift in diversification would not be detected in a family-level analysis, and it is important to note that taxonomy plays a large role in such analyses. While some analyses (which have contributed to the supertree presented here) have shown Serritermitidae to be a stand-alone group (Donovan et al., 2000; Kambhampati & Eggleton, 2000; Thompson et al., 2000) justifying family rank, other phylogenies show it nested within other families such as Rhinotermitidae (Inward et al., 2007b), calling into question their validity. Cancello & De Souza (2005) expanded the Serritermitidae to include the two described species of Glossotermes; G. oculatus and G. sulcatus. If we accept this and make Serritermitidae a three-species family, there is no effect on the results presented here, and a negative shift is still observed in the Serritermitidae lineage. Additionally, the imago-worker mandibles of Glossotermes are morphologically similar to those of S. serrifer, perhaps representing a particular dietary habit. Furthermore, G. oculatus has


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been shown not to build its own nests, and instead secondarily use those of Coptotermes (Apolina´rio & Martius, 2004). Lastly, little is known about Serritermitidae societies. There are no available figures on colony size, but even if they have a colony size < 106 (perhaps linked to their restricted lifestyle), the positive shift in the Kalotermitidae + Serritermitidae + Rhinotermitidae + Termitidae lineage as a whole, coinciding with an increase in colony size, is still valid, as this shift precedes the negative shift in the Serritermitidae. Ancestral state analyses in general show a great deal of uncertainty compared with a parsimony analysis applied to the same tree, which would for example show the ancestor to all termites to be a wood feeding, wood nesting creature living in small colonies, although whether it had a true worker caste and its foraging strategy are still unknown (Grandcolas & D’Haese, 2002, 2004). However, parsimony approaches are not amenable to significance tests, and hence it is difficult to assign confidence to such reconstructions. The likelihood approach uses more information (e.g. branch lengths) and explicit models of evolution. However, likelihood approaches are certainly not a panacea either. One problem is that they may become less accurate if the phylogenetic information is incomplete (Mooers & Schluter, 1999). This is because they work through explicitly estimating evolutionary transition rates from the data, and phylogenies omitting branches may therefore produce bias. Of course parsimony analyses also have to make assumptions about transition probabilities (or costs); it is just that these are assumed rather than estimated from the data, and normally implicitly assumed to be equal. Clearly therefore, the more complete the phylogeny, the more reliable the ancestral state reconstructions are likely to be. Dictyopteran relationships Our supertrees suggest broad underlying agreement between existing phylogenetic studies in ordinal relationships, with Mantodea sister to Blattaria and Isoptera, but most importantly Isoptera are shown to nest within ‘Blattaria’ in all analyses. Cryptocercidae, so often hypothesized to be the sister group to Isoptera are supported as such, in agreement with the recent study of Ware et al. (2008), not included in our supertree, which is perhaps the closest study to a supermatrix of the Dictyoptera based on four genes and 175 morphological characters. Although Ware et al. (2008) present four trees using either parsimony or Bayesian analysis and with varying outgroup selection, we find reasonable agreement between our supertree topology and the topologies they present: 1. The relationships of Mantodea, ‘Blattaria’ and Isoptera as recovered by the analyses of Ware et al. are as for our supertree, except for one Bayesian analysis suggesting a novel hypothesis where Mantodea are also nested within ‘Blattaria’.

2. The supertree suggests that Mantodea and Isoptera form true monophyletic clades. 3. Within Mantodea, relationships are difficult to resolve (particularly in Ware et al.’s Bayesian analyses), and some families are even shown not to be monophyletic. However, in the parsimony analyses of Ware et al., where Mantodea are more resolved the supertree agrees with a clade comprising Mantidae (except two taxa in Ware et al., which come out more basal), Hymenopodidae and Empusidae. Amorphoscelidae is sister to this clade and although Ware et al. present a different rearrangement of lineages, we agree that Chaeteessidae, Mantoididae and Metallyticidae are the first families to split from the rest of Mantodea. 4. Within ‘Blattaria’ and Isoptera, our supertree supports the sister group relationship between Cryptocercidae and Isoptera, as well as the grouping of Blaberidae and Blatellidae, and the relationship between Polyphagidae and Nocticolidae (even though this clade as a whole is not consistently place in their trees). Mastotermitidae is recovered as sister to other Isoptera in their parsimony analyses. The Mantodea are the most problematic order in the Dictyoptera to resolve. It is probable that some of the families traditionally recognized are not monophyletic and this family-level phylogeny provides a simplified overview of their relationships. The Mantodea in input trees required much attention in treating polyphyletic taxa and a solid taxonomy would be invaluable for this order. Furthermore, mantodean phylogenies are sparse and are further highlighted here as an area of focus for future phylogenetic research. Dates of origin We dated the Isoptera tree using two methods to test the robustness of diversification rate and ancestral state analyses. The results of these diversification tests did not depend on the dates used, but incidentally, the dating gave unexpected results suggesting earlier origins for some clades than has previously been suggested. It would be premature at present to suggest that one of these dating schemes is more closer to the truth than the other, but the results merit discussion given the interest surrounding traditional and molecular dating methods (Benton & Ayala, 2003; Marshall, 2008). Using fossil dates the origin of modern Dictyoptera is dated at 203.5 Mya (early Jurassic) based on a minimum first appearance date of the proposed fossil sister group Blattulidae. This fossil family is presented by Grimaldi & Engel (2005) as the outgroup to modern Dictyoptera, whereas other authors have suggested (although not in a phylogeny), alternatives. For example, Maekawa et al. (2005) consider Mesoblattinidae as the extinct sister group to modern Dictyoptera and consequently suggest a different date of origin (135–180 Mya). More in line with their estimate is the date given here for the divergence



of the Mantodea from the ‘Blattaria’ + Isoptera at 185.6 Mya. Whichever of these fossil dates is considered the origin of modern Dictyoptera, all point to a Jurassic origin. It is also worth considering that previous molecular dates correspond roughly to fossil dates for the Dictyoptera. Lo et al. (2003) suggest that modern Dictyoptera split from their fossil roachoid ancestors in the early-mid Jurassic, with the split between Mantodea and ‘Blattaria’ + Isoptera occurring in the late Jurassic. Our analyses however point to an earlier date for these events, because the most complete fossil record (according to the criteria used) belongs to a family that includes Cretaceous fossils, whilst the molecular tree (Thompson et al., 2000) suggests that this is a relatively derived split with deeper divisions further down the tree. The suggestion of Ordovician Dictyoptera, gained using 95% confidence intervals on the molecular dates, is clearly out of line with palaeontological estimates (Grimaldi & Engel, 2005) showing Hexapod origins in the Devonian. We regard these dates as inherently too liberal as described above, but then they are designed to be liberal (Marshall, 2008). However, we believe that the suggestion of Triassic (or even earlier) Isoptera deserves further attention. Supposed termite nest fossils have been reported as early as this (Hasiotis & Dubiel, 1995). Knowing the true age of the crown Dictyoptera will come with a better understanding of the roachoid lineages leading to the modern orders, and could be aided by evidence from further genes.

Conclusions Termites provide evidence that eusociality is not necessarily a hindrance to species richness, in contrast to the general suggestion of Wilson (1992). It remains to be seen to what extent this is also true for other eusocial groups of insects, and thus how generally it might hold, but it fits with other suggestions of increases in diversification within other eusocial groups (Moreau et al., 2006), and reports of high rates of molecular evolution (Luchetti et al., 2005). In turn, this study begs questions about speciation and extinction processes in eusocial insects and how eusociality might have promoted the former or, perhaps less likely, reduced the latter. In turn, this will likely require models and mechanistic empirical studies of the speciation process, which can consider how eusociality affects resource exploitation, ecological coexistence, population divergence and reproductive isolation.

Acknowledgments R.B.D. was supported by BBSRC PhD studentship BB ⁄ D527026 ⁄ 1. The authors thank Graham Thompson for access to the dataset of Thompson et al. (2000) and Xavier Bailly for advice and useful discussion in constructing the molecular phylogeny.

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Supporting information Additional supporting information may be found in the online version of this article: Appendix S1 List of the 26 input trees used in the final analysis and any remaining data non-independence between them. Appendix S2 Materials and methods: input tree search criteria, software settings, supertree dating methods, diversification analyses used, method for ancestral state reconstruction and log likelihoods for one and two-rate models for each trait. Appendix S3 Fossil dates for dictyopteran families and pure birth rate comparisons. Appendix S4 Species richness comparisons for sister taxa. Appendix S5 Probabilities and log likelihoods for state of traits at ancestral nodes. Please note: Wiley-Blackwell are not responsible for the content or functionality of any supporting materials supplied by the authors. Any queries (other than missing material) should be directed to the corresponding author for the article. Received 30 March 2009; revised 11 May 2009; accepted 14 May 2009
