Blattaria

Zrzavý, Jan, 2008, Four chapters about the monophyly of insect ‘ orders’: A review of recent phylogenetic contributions, Acta Entomologica Musei Nationalis Pragae 48 (2), pp. 217-232 : 220-222

Blattaria and Isoptera: the origin of eusociality

Termite societies are large, extended families with a characteristic division of labor and with only a few reproducing individuals within a colony. Termites (Isoptera) are the earliest-evolved eusocial insects, with their complex societies dating back to the Cretaceous (130 million years ago). They are closely related to the cockroaches ( Blattaria ) and mantids (Mantodea), forming a well-established clade, the Dictyoptera , uniquely defined by having a ‘perforated’ tentorium, proventriculus with six internal longitudinal plicae, asymmetrical male genitalia (in details of uncertain homology – see disputes of, e.g., GRANDCOLAS (1996) versus KLASS (2001)), and reduced ovipositor, and by enclosing their eggs with secretions from the colleterial glands within an ootheca (lost in most termites; see NALEPA & LENZ (2000), COURRENT et al. (2008); for termite phylogeny see INWARD et al. (2007a,b), LEGENDRE et al. (2008)). Within the Dictyoptera , there is agreement that both termites and mantids are monophyletic groups. Although the relative positions of these lineages is somewhat debated, the weight of the evidence strongly suggests that the termites are nested within the Blattaria , being just ‘highly modified, social, myopic, wood-eating roaches’, or ‘citizen roaches’ (GRIM- ALDI & ENGEL 2005). It is then clear how misleading it was to use termites as an outgroup in previous analyses of the blattarian phylogeny, which excluded them a priori from nesting within the cockroaches.

The morphology-based phylogeny of blattarian families was explored, e.g., by GRANDCOLAS (1996), GRANDCOLAS & D’HAESE (2001), KLASS (2001), and KLASS & MAIER (2006). The major contributions agree that the basalmost divergence is between the Blattidae (possibly paraphyletic; see KLASS (2001), KLASS & MAIER (2006) and references therein) and the rest of roaches, and that the Blattellidae and the Blaberidae form a clade. The Polyphagidae are placed somewhere between basal blattids and the blattelid-blaberid clade; the genus Cryptocercus Scudder, 1862 , is the subject of the greatest disparity between the published phylogenies. By all means, it is related to the Polyphagidae , either as its deeply nested member (and consequently not related to the termites; see GRANDCOLAS (1993), GRANDCOLAS & DELEPORTE (1996)), or forming together with the termites a sister group of the polyphagids (see KLASS & MAIER 2006).

The relict wingless, long-lived, and social ‘woodroach’ Cryptocercus is then one of the most intriguing insect genera. There are several species living in forests of North America and East Asia. Usually a pair of parents and about 20 offspring inhabit galleries in a soft, rotten log, remaining together for at least three years (the brood care probably lasts until the death of the adults), with larvae maturing in approximately six years (see NALEPA & BANDI (2000), KAMBHAMPATI et al. (2002) and references therein). The juveniles are pale, termite-like, with highly reduced eyes, and they feed on liquids exuded by an adult from the anus (proctodeal trophallaxis) for approximately their first year (1st and 2nd instars). This behaviour allows them to acquire symbiotic oxymonadid and hypermastigid protists, required for the digestion of wood. Young larvae actively groom older juveniles and adults.

An overwhelming molecular evidence from recent years ( LO et al. 2000, 2003, 2007; TERRY & WHITING 2005; KJER et al. 2006; PELLENS et al. 2007; INWARD et al. 2007a; LEGENDRE et al. 2008; WARE et al. 2008) shows that the Isoptera are a sister group of Cryptocercus . The most comprehensive molecular analysis by INWARD et al. (2007a) included 107 species of the Dictyoptera (five of the 15 mantid families, all six cockroach families as well as 22 of the 29 cockroach subfamilies, and all termite families and subfamilies), along with 11 outgroups, and five gene loci (two mitochondrial: 12S rDNA and cytochrome oxidase II, three nuclear: 28S rDNA, 18S rDNA, and histone 3). The Isoptera- Cryptocercus clade was found as sister to the Blattidae , and that combined clade as sister to the Blattellidae + Blaberidae . The Polyphagoidea ( Polyphagidae + Nocticolidae ) are then sister to all the other cockroaches (including the termites). Similar phylogenetic patterns have been received from an analysis of the bacterial intracellular symbionts ( Blattabacterium Mercier, 1906 ) that reside in specialized cells of cockroaches and the basalmost termite Mastotermes Froggatt, 1897 ; the analysis found a close relationship between endosymbionts from termites and woodroaches ( LO et al. 2003).

WARE et al. (2008) showed, using four gene loci (cytochrome oxidase II, 16S rDNA, 18S rDNA, and 28S rDNA) and morphological data for 62 species (including eight outgroups), that the choice of both outgroup and ingroup taxa as well as data partition greatly affects tree topology. Depending on the outgroup selection, the most basal splitting event within the Dictyoptera is either between the Mantodea and the Blattodea (cockroaches and termites), or between the Polyphagoidea and the rest of the Dictyoptera (including mantids). Within the non-polyphagoid Blattodea , the next problematic issue is the relationship among the Blattellidae + Blaberidae , Blattidae , and Cryptocercus + Isoptera (probably a sister group of the blattids).

This is in strong contrast to earlier hypotheses that assumed a position of the Isoptera outside a monophyletic Blattaria ( THORNE & CARPENTER 1992) and a subordinate position of Cryptocercus inside the cockroach family Polyphagidae (GRANDCOLAS 1996) . In all molecular analyses all included species of the Polyphagidae ( LO et al. 2003, 2007; KJER et al. 2006; INWARD et al. 2007a,b; KLASS et al. 2008; LEGENDRE et al. 2008; WARE et al. 2008) clustered together unambiguously, while the whole polyphagid clade is remote from the Cryptocercus -Isoptera clade. Consequently, the hypothesis of Cryptocercus being deeply nested in the Polyphagidae (close to Therea Billberg, 1820 ) should eventually be dismissed. The only evidence that may still contradict a Cryptocercus- Isoptera clade is the analysis of hypertrehalosaemic neuropeptides from corpora cardiaca ( GÄDE et al. 1997), but this is based on very few informative characters.

Morphologically, the sister-group relationship between Cryptocercus and Isoptera is based on the morphology of the proventriculus, dentition of the mandibles, possibly also detailed structure of the antennal segments, relatively small genome size ( KOSHIKAWA et al. 2008), and predominantly on numerous behavioural and ecological characters (see KLASS et al. (2008) for a review). They include shared (and unique) ability to nest in and ingest fairly recalcitrant dead wood sources that may take decades to degrade. All studied cockroach and termite species have endogenous cellulase genes, which suggests a widespread ability to use cellulose-based materials as food. Only Cryptocercus and lower termites, however, have an additional specific type of cellulose digestion that involves hindgut symbiotic flagellates, requiring vertical intergenerational transmission. Cryptocercus and lower Isoptera share many flagellates of the Oxymonadida and Hypermastigida (both Excavata) in their hindgut that are unique to them, such as the Spirotrichosomidae , Hoplonymphidae , Staurojoeninidae , and Eucomonymphidae . GRANDCOLAS (1999a,b) and GRANDCOLAS & DELEPORTE (1996) assumed that xylophagy and intestinal symbiosis in the Isoptera and Cryptocercus was a matter of convergence and/or horizontal transfer (gut flagellates could have been passed from termites to Cryptocercus ). Interestingly, several groups of the hindgut flagellates are shared exclusively between Cryptocercus and different isopteran subgroups ( Leptospironympha Cleveland, 1934 and the Spirotrichosomidae shared with the Stolotermitinae; Oxymonas Janicki, 1915 , Hoplonymphidae and Staurojoeninidae shared with the Kalotermitidae , and the Eucomonymphidae shared with the Rhinotermitidae ). The differences in hindgut flagellate faunas of the various termite subgroups have probably been caused by mosaic-like losses from the ancestrally complete set of oxymonadids and hypermastigids (even recent, intraspecific losses have been reported; see KLASS & MEIER (2006)).According to the lateral-transfer hypothesis, Cryptocercus should have obtained its gut fauna either through several additive tranfers from a variety of termite groups, or through a single transfer from the termite ancestor. If Cryptocercus were of Cenozoic origin ( GRANDCOLAS 1999a,b), its physical contact with the isopteran stem lineage would be impossible; several parallel contacts between cryptocercids and termites leading to sequential collection of the Cryptocercus hindgut fauna are unparsimonious at best. Recently, OHKUMA et al. (2008), based on18S ribosomal DNA and glyceraldehyde-3-phosphate dehydrogenase sequences of the woodroach and termite trichonymphid symbionts (Hypermastigida), found that the symbionts of Cryptocercus were always robustly sister to those of termites. It strongly suggests that this set of symbiotic flagellates was already present in the common ancestor of Cryptocercus and the Isoptera.

As concerns their social behaviour, Cryptocercus and the Isoptera share monogamy, extended biparental care, allogrooming, and proctodeal trophallaxis. The Cryptocercus -like biparental sociality is also present in dealated pairs of termites during the early stages of colony foundation; the family switches to eusociality with the appearance of workers or pseudergates. The crucial difference in the sociality of Cryptocercus and termites is that only in the latter is the care and feeding of young brood taken over by older brood in the family. However, as a result of asynchronous hatching and the quick growth of neonates, both trophically dependent (1st and 2nd instars) and trophically independent nymphs (3rd and subsequent instars) can be contemporaneous even in young families of Cryptocercus ( KLASS & MEIER 2006) .

The finding that the termites are nested within the cockroaches causes a classificatory problem. INWARD et al. (2007a) proposed that the ‘Isoptera’ should no longer be used and that the species should be classified within the family Termitidae as part of the order Blattodea . This would mean that the existing termite taxa need to be downgraded by one taxonomic rank (i.e. families become subfamilies, subfamilies become tribes etc.), a taxonomical action that provoked strong counteraction (‘Save Isoptera!’; LO et al. 2007). In fact, there is no reason why not to preserve the well-known and widely used name ‘Isoptera’ regardless of its phylogenetic position; naturally, this problem is a direct consequence of using the basically non-phylogenetic Linnean rank hierarchy in the phylogeny-dominated modern systematics.