‘One piece’ (= OP) termites are thought to display the basal ecological condition in the group (Roisin, 2000 ); a single piece of wood serves as both food and nest (Abe, 1987 ). Despite their basal nesting ecology, however, extant OP termites display a full range of derived characters. These include the existence of a sterile terminal caste (soldiers), philopatric reproduction by secondary reproductives (neotenics or soldier‐neotenics), division of labour, arrested development and extreme phenotypic plasticity of helpers (= alloparents), interdependence of colony members because of the death of symbiotic gut protists during the host molting period, and a small body size and thin, unsclerotised cuticle (Nalepa, 2011a ,b). OP termites have clearly passed Wilson and Holldobler's ( 2005 ) ‘point of no return’: an individual can neither persist nor reproduce independently of the colony (Eggleton, 2011 ; Lo & Eggleton, 2011 ). While established colonies of extant termite species are valid and useful as models for examining the elaboration and maintenance of termite eusociality, they cannot be used in proposing its origins. Selection pressures associated with early social evolution are rarely the same as those currently maintaining and driving it (Linksvayer & Wade, 2005 ; Hunt, 2012 ; Falk et al., 2014 ) because eusociality fundamentally changes the nature of clades (Inward et al., 2007b ). The use of extant termites as models of the ancestor assumes a modern, eusocial life history as the selective background and has led to a strong conceptual bias regarding the nature of their evolutionary trajectory.

The unequivocal sister group status of Crytocercus to the termite clade (Engel et al., 2009 ) indicates that behaviours, symbiotic associations, and social structure common to Cryptocercus and termites are most parsimoniously interpreted as homologies and can be used to test ideas of early termite evolution (Deitz et al., 2003 ; Klass et al., 2008 ; Lo & Eggleton, 2011 ). The majority of current treatments of the origin of termite eusociality nonetheless use extant termite species as models of their own ancestral state. These studies fail to recognise that eusociality is a shared‐derived character of termites, and undoubtedly the key innovation that allowed their biology to veer sharply away from that of their cockroach relatives (Nalepa, 2011a ).

It has long been proposed that termites and cockroaches are close relatives (e.g. Cleveland et al., 1934 ; McKittrick, 1965 ; Lin & Michener, 1972 ), but the relationship was not clarified until the turn of the millennium. In 2000, Lo et al . ( 2000 ) published evidence that termites are a monophyletic clade embedded within cockroaches, and sister group to the wood‐feeding, subsocial cockroach genus Cryptocercus . Subsequent studies strongly support this placement, reflected in phylogenies based on morphological and molecular characters of the insects, phylogeny of symbiotic bacteria in the fat body, and the phylogeny of their hindgut protists and associated bacterial ectosymbionts (Deitz et al., 2003 ; Lo et al., 2003 ; Inward et al., 2007a ; Ware et al., 2008 ; Carpenter et al., 2009 ; Davis et al., 2009 ; Ikeda‐Ohtsubo & Brune, 2009 ; Ohkuma et al., 2009 ; Cameron et al., 2012 ; Djernaes et al., 2012 ; Dietrich et al., 2014 ; Tai et al., 2015 ). These results challenge the ordinal status of termites, and taxonomic nomenclature has shifted accordingly. The order Blattodea is now comprised of termites (epifamily Termitoidea) together with all cockroach taxa (Beccaloni & Eggleton, 2013 ). The fundamental outcome is clear: termites are eusocial cockroaches.

In summary, there were two levels of dependence in an ancestor. The first was interdependency of the host and its range of microbial gut mutualists, together forming a chimera resulting from the expression of multiple interacting genomes (Vavre & Kremer, 2014 ). The second dependency was obligate subsociality. Once committed to an altricial developmental track, brood care becomes obligatory, because neonate survival is nil in the absence of care (Wesolowski, 1994 ).

As a non‐eusocial cockroach, the termite ancestor had one developmental track: a linear, progressive hemimetabolous development to the adult stage, responsive to environmental conditions but without alternate pathways. As a wood‐feeding cockroach, that development was prolonged: development takes up to 3 years in the genus Salganea (Maekawa et al., 2008 ); 4–6 years in Panesthia cribrata Saussure (Rugg & Rose, 1990 ); and up to 7 years in Cryptocercus clevelandi Byers (Nalepa et al., 1997 ). These three wood‐feeding cockroach genera have also converged on a large body size and robust morphotype in adults, supporting the suggestion that the cockroach ancestor of the termites also displayed these characteristics.

The life history characters shared by Cryptocercus and incipient colonies of OP termites are homologous and should be considered a feature of their common ancestor (Fig. 1 ). Most notably, the ancestor had obligate biparental subsociality, inextricably linked to host dependence on gut symbionts, the need to transfer those symbionts between generations, nutritional dependence and vulnerability of neonates, and consequently, costly parental care. These constitute an integrated, covariant character set (Fig. 1 b), one in which individual components cannot respond to selection without changing another trait that also contributes to fitness. As such, they are expected to respond to selection pressures as a module (McKinney & Gittleman, 1995 ; Flatt & Heyland, 2011 ; Davidowitz et al., 2012 ; Murren, 2012 ).

The gut symbionts inherited from a common ancestor require vertical intergenerational transmission in both Cryptocercus and OP termites (Nalepa et al., 2001 ; Ohkuma et al., 2009 ). The digestive tract of neonates is free of microbes, and establishment of the full complement of mutualists is an extended and sequential process; it varies in length between species, but typically is not complete until the third instar (Kitade et al., 1997 ; Inoue et al., 2000 ). Bacteria are established first, followed by the smaller flagellates, and finally, the large flagellate genera that not only phagocytose host‐ingested wood particles, but also are host to nitrogen‐fixing bacteria that densely cover their surface (Grassé & Noirot, 1945 ; Nalepa, 1990 ; Kitade et al., 1997 ; Noda et al., 2006 ; Carpenter et al., 2011 , 2013 ). Young instars initially have a ‘completely dependent nutrition’ but progressively become competent feeders (Noirot & Noirot‐Timothée, 1969 ). Until then, they rely on repeated trophallactic transfer of gut fluids from an adult for gut symbionts, as well as for energy and nutrients ultimately derived from the wood diet and symbionts of the parents.

Parental behaviour inevitably imposes costs on parents (Trivers, 1972 ; Tallamy & Wood, 1986 ; Gilbert & Manica, 2010 ; Royle et al., 2012 ); it does so most profoundly in animals with altricial offspring (Ricklefs, 1974 ; May & Rubenstein, 1984 ; Clutton Brock, 1991 ), and those that live in marginal habitats (Galef, 1983 ; Tuomi et al., 1983 ). Cryptocercus and OP termites fall into both categories. The transfer of trophallactic food to neonates, as well as non‐food parental support such as excavating galleries, sanitation activities, and defence against conspecifics and predators exacts a physical toll in both taxa. Adults in young families lose weight, stored protein is markedly reduced, and oogenesis slows or stops (Morgan, 1959 ; Maki & Abe, 1986 ; Nalepa, 1988b ; Shellman‐Reeve, 1994 ; Johnston & Wheeler, 2007 ).

Neonates in both Cryptocercus and in OP termites are small, soft, crushable, edible, vulnerable to pathogens and desiccation, and unable to feed themselves; their mandibles are delicate and unsclerotised, and they lack the symbiotic associations required for processing a cellulose‐based diet (Grassi & Sandias, 1897 ; Grassé & Noirot, 1945 ; Buchli, 1958 ; Rosengaus & Traniello, 1993 ; Nalepa et al., 2008 ). Because they are so frail, first and second instars are rarely used in termite behavioural studies (e.g. Cabrera & Rust, 1999 ). The fragility and dependence of early post‐hatch stages makes brood care obligate in Cryptocercus , as well as in extant colonies of OP termites (Wilkinson, 1962 ; Mensa‐Bonsu, 1976 ; LaFage & Nutting, 1978 ; Lenz, 1987 ; Waller & LaFage, 1987 ; Shellman‐Reeve, 1990 ; Kitade et al., 1997 ; Machida et al., 2001 ; Crosland et al., 2004 ); contra Korb ( 2007 , 2009 ); Korb et al . ( 2012 ). Altricial development in the early instars of these taxa suggests that it was an established feature of ancestral life history prior to the origin of termite eusociality (Nalepa, 2010 ).

The social structure of Cryptocercus is the equivalent of a newly founded termite colony (Seelinger & Seelinger, 1983 ; Nalepa, 1994 ). Adults excavate the nest, plug gaps, construct barriers, clean galleries, remove frass and fungi from the vicinity of the nursery, and bury the inedible dead (Bell et al., 2007 : fig. 9.4; Nalepa, 1988a ). After hatch, adults feed the first few instars on hindgut fluids (proctodeal trophallaxis); the dry weight of dependent nymphs increases by more than an order of magnitude between the first and second instar (Nalepa & Mullins, 2009 ). Nymphs are nutritionally independent at the third instar, but parental care typically continues until the death of adults. Parents defend galleries against intruders, frequently alerted to their presence by alarm (‘jerking’) behaviour of the young cockroaches (Seelinger & Seelinger, 1983 ; Park & Choe, 2003 ). There is extensive physical contact of the young nymphs with adults, not just during trophallaxis and grooming, but also during inactive periods. Seelinger and Seelinger ( 1983 : fig. 4) illustrate 10 young nymphs surrounding, oriented to, and in contact with abdomen of an adult.

There are few solitary cockroaches (Bell et al., 2007 ), and no solitary termites. The tenet that there are no subsocial termites, however, is not entirely true. All independently founded termite colonies begin as a biparental family, which then makes a gradual transition to eusociality during early colony ontogeny. As such, it is widely accepted that the termite ancestor was subsocial, and lived in biparental family groups (Wheeler, 1928 ; Kennedy, 1966 ; Noirot, 1985 ; Noirot & Pasteels, 1987 ; Nalepa, 1988b , 1994 ; Roisin, 1990 ; Thorne, 1997 ; Klass et al., 2008 ). By definition, then, the baseline social system was defined by parental care.

In general, the nesting ecology of Cryptocercus is like that of dampwood termites (Abe, 1987 ; Nalepa, 2003 ); both taxa require the relatively moist conditions associated with rotting logs on the forest floor (Collins, 1969 ; Lenz, 1994 ). Although they have an OP nesting strategy, kalotermitids such as Cryptotermes spp. are ecologically derived in that they live in relatively dry wood of a restricted volume, such as dead branches and scar tissue on standing trees (Abe, 1987 ; Lenz, 1994 ). They are desiccation tolerant, as they typically lack access to free water (e.g. Collins, 1969 ), and their mandibles are enriched with zinc as an adaptation to their dry, mechanically difficult food source (Cribb et al., 2008 ). Collins ( 1989 ) suggested that competitive exclusion by higher termites (Termitidae) confined drywood termites to dead limbs in the canopy. Kalotermitidae lack the microbe‐rich environment characteristic of a damp log on the forest floor (Rosengaus et al., 2003 ), which in turn strongly influences food quality and pathogen pressure. As ecological patterns are not independent of evolution (Pelletier et al., 2009 ; Nowak et al., 2010 ; Van Dyken & Wade, 2012 ; Hernandez et al., 2013 ), a damp, rotting log best supplies the framework for understanding the selective pressures and phenotypes that maximised fitness when cockroaches crossed the subsocial to eusocial divide.

The idea that the first termites were wood‐boring insects that found both food and shelter within logs and stumps has a long history (Emerson, 1938 ; Noirot & Pasteels, 1987 ; Noirot, 1992 ) and was brought into focus by Abe's ( 1987 ) insights into the relationship between the number of sterile castes in a given termite taxon and its nesting strategy. Like termites in the Archotermopsidae and Kalotermitidae, the ecology of Cryptocercus is also OP, i.e. they nest within their food source. Once the male‐female pair bond is established in these cockroaches, their subsequent family life takes place entirely within a single log.

In contrast, nest inheritance scenarios (Thorne et al., 2003 ; Korb, 2007 , 2009 ; Johns et al., 2009 ; Howard et al., 2013 ) are predicated on helpers ‘delaying dispersal’ with the incentive of becoming neotenic reproductives upon the death of the king or queen in the termite colony, consequently allowing them to inherit the nest and the workforce. Three points argue against this hypothesis. First, it assumes that a workforce (i.e. division of labour) was already in place. Second, neotenics (and soldier‐neotenics) are derived developmental options, and like soldiers, are dependent on alloparental care (e.g. Nagin, 1972 ; Greenberg & Stuart, 1979 ; Lenz, 1987 ). Third, given the probable life history characteristics of the ancestor, juveniles did not need ‘special incentives’ to remain in the natal nest. Because of their long developmental times, young nymphs were not capable of independent reproduction either inside or outside the nest, and their vulnerable, altricial morphology would make it unlikely they would leave the protective environment provided by the parents and the natal log. Field studies of Cryptocercus punctulatus Scudder indicate that young cockroaches do not begin venturing away from their family and nest until they are about half grown, have a melanised cuticle, and are at least 3 years old (Nalepa & Grayson, 2011 ).

If the ancestor possessed all of the characters listed in Fig. 1 , then ‘Fortress Defence’ and ‘Nest Inheritance’ scenarios for the origin of termite eusociality cannot be supported. Soldiers were the first sterile caste to appear in termites (Noirot & Pasteels, 1987 , 1988 ); as such, it is often suggested that defence of the food/shelter habitat was a strong selective pressure leading to eusociality in the lineage (Strassmann & Queller, 2007 ; Korb et al., 2012 ). In Cryptocercus as well as in other subsocial wood‐feeding cockroaches, however, defence is a component of parental care, and adults are heavily armoured, aggressive defenders. Extant termite soldiers are furthermore a dependent caste (Snyder, 1926 ; Noirot & Darlington, 2000 ; Buczkowski et al., 2007 ), suggesting that alloparental feeding was a prerequisite for their full evolutionary differentiation (Nalepa, 2011a ). Although the termite ancestor lived in a log that can be considered a defensible fortress, it was parents that defended it.

It follows that hypotheses of the origin of termite eusociality have to be examined within the context of the environmental factors that have a strong influence on the development of young cockroaches. Evolutionary modification of development needs to occur within the conservative ancestral ontogeny (Raff, 1996 ), and analysed in a life history framework that incorporates not only the specific ecological environment (van der Weele, 1999 ; Atkinson & Thorndyke, 2001 ; Gilbert, 2005 ; Sultan, 2007 ; Braendle et al., 2011 ), but also, and of particular relevance here, the environment experienced by juveniles (Kasumovic, 2013 ).

Morphogenesis in OP termites is characterised by weak or delayed post‐embryonic development, with the majority of colony members arrested in the small, soft‐bodied, altricial morphotype characteristic of young juvenile stages of their cockroach ancestors (Nalepa, 2011a ,b). The origin of termite eusociality, then, is best framed not as the suppression of reproduction in adults, but as the control of development in juveniles. In extant OP termites, differentiation to a terminal caste such as a soldier or reproductive of any type requires developmental progression via one or more additional molting cycles (Noirot & Pasteels, 1987 ; Noirot, 1990 ).

Like coprophagy, proctodeal trophallaxis spans the nutritional, microbial, and social environments but with broader scope and deeper impact. First, unlike coprophagy, proctodeal trophallaxis requires physical contact and behavioural interaction (McMahan, 1969 ; Nalepa & Bandi, 2000 ; Nalepa et al., 2001 ). Second, the behaviour allows for interindividual transfer of materials that would otherwise degrade in the outside environment. This includes the trophic stages of gut protists, and hormones, enzymes, metabolites, and other chemicals that may serve as physiological or behavioural signals. Third, it is impossible to separate symbiont transfer from nutrient transfer during proctodeal trophallaxis because the symbionts themselves also serve directly as food. Both gut flagellates damaged by the proventriculus and bacteria lysed in the foregut are utilised as nutrients by the recipients of proctodeal fluids (Grassé & Noirot, 1945 ; Grassé, 1952 ; Fujita et al., 2001 ; Machida et al., 2001 ; Tokuda et al., 2014 ).

The influence of gut microbes extends beyond the boundaries of the host body via coprophagy (i.e. ingestion of feces), a complex, multifactorial behaviour distinct from proctodeal trophallaxis. A faecal pellet can be a source of microbial protein, but is also a mechanism for transmitting the resistant stages of prokaryotes, as well as semiochemicals and metabolites originating with the excretor and all its gut mutualists (Nalepa et al., 2001 ; Bell et al., 2007 ). Faecal pellets play a role in sanitising the nest (Rosengaus et al., 1998b , 2013 ) and also serve as bricks and mortar to plug holes and gaps, to build pillars and walls to partition galleries, and to erect barriers when galleries approach those of conspecifics adjacent in the log (Bell et al., 2007 : fig. 9.4).

Allogrooming is an interaction of the social environment with the microbial pathogens in a rotting wood nest. The behaviour is characteristic of both young Cryptocercus (Seelinger & Seelinger, 1983 ) and termites, and facilitates disease resistance by removing spores and by spreading salivary antifungal compounds (Rosengaus et al., 1998a ; Bulmer et al., 2012 ). Allogrooming is also a source of tactile stimuli, a mechanism of disseminating contact pheromones (Costa‐Leonardo & Haifig, 2010 ), and is thought to play a role in termite caste determination (Maistrello & Sbrenna, 1998 ; Maekawa et al., 2012 ). The behaviour also overlaps with the nutritional environment if the groomer ingests spores, cuticular hydrocarbons, and externally attached debris.

The nutritional, microbial, and social environments are each known to interact with cockroach physiology and development and are in many aspects strongly specific to the Cryptocercus ‐termite lineage. A wood diet, an extraordinarily convoluted relationship with gut symbionts, and hemimetabolous biparental subsociality with altricial offspring is a rare combination. Each of these environments may act alone or in tandem, directly or indirectly, and with complex and overlapping interactions. Food derived from conspecifics in the log galleries, including faeces, exuvia, corpses, and exudates (Nalepa, 1994 : Table 3.1) originates from the social environment but crosses over into the nutritional environment. Similarly, tearing wood free from the log and reducing it to a size suitable for ingestion is a costly, energy consuming process (Watanabe & Tokuda, 2010 ) that is best done communally (Nalepa, 1994 : fig. 3.1).

Internally, Cryptocercus and termites are the ‘poster children’ for nutritional symbioses, as they have the most elaborate, interactive gut community of any insect (Engel & Moran, 2013 ). Studies have grown exponentially since the advent of molecular sequencing, and a large number of gut phylotypes or species have been identified (Brune & Ohkuma, 2011 ; Ohkuma & Brune, 2011 ; Brune, 2014 ). Functionally, gut microbiota partner with the host and each other to interactively degrade plant polymers, fix atmospheric nitrogen, synthesize amino acids, and recycle nitrogenous waste products (Potrikus & Breznak, 1981 ; Bentley, 1984 ; Higashi et al., 1992 ); the latter is possible because the hindgut is a component of both the digestive and the excretory system (Mullins, 2015 ). Gut microbes play a role in kin recognition within the social group (Matsuura, 2001 ; Lize et al., 2013 ), in reducing the risk of mycosis at the individual and colony level (Rosengaus et al., 2013 , 2014 ), and may directly affect insect development by regulating gene expression in their host (Cruden & Markovetz, 1987 ; McFall‐Ngai, 2002 ; Gilbert, 2005 ). This sophisticated internal microbial community is clearly and strongly tied to host fitness (e.g. Rosengaus et al., 2011b ), yet is rarely considered in contemporary hypotheses of the origin of termite eusociality.

Termites are strongly distinguished from other major eusocial insects by their food: a cellulose‐based diet requires extensive, sequential processing that involves not only physical and chemical manipulations by the host but the participation of multiple interacting symbionts (LaFage & Nutting, 1978 ; Waller & LaFage, 1987 ). The ancestor faced two serious problems in using this food source: the decomposition of cellulose and the acquisition of sufficient nitrogen for reproduction and development (Higashi et al., 2000 ). Because of the strong carbon–nitrogen imbalance characteristic of their diet, wood feeders can either (i) consume mass quantities of wood and eliminate the excess carbon or (ii) add nitrogen. Because OP termites need to consume wood prudently or risk destroying their nest, mechanisms of nitrogen acquisition and conservation are crucial to this nesting type (Higashi et al., 1992 ). A second consequence of an OP lifestyle is that the diet of both parents and offspring is fixed when adults pair up and select the nest. Although there is always some nutritional variation within a given log (e.g. Shellman‐Reeve, 1994 ) an OP ancestor forfeits the opportunity to range more widely within the habitat to seek specific nutrients as reproductive and developmental needs change; this is a behaviour common in non‐wood feeding cockroaches (Mullins & Cochran, 1987 ; Bell et al., 2007 ).

Parents supplied all requisites of life to hatchlings in the termite ancestor, and neonates co‐evolved to function within that social environment. Comprehensive parental care relaxed selection for protective and nutrient gathering structures in their offspring, resulting in the dependence currently exhibited by early instars of both Cryptocercus and OP termites. Altricial development of neonates was the first deviation from standard hemimetabolous development in the termite ancestor and a prerequisite for the subsequent transition to eusociality (Nalepa, 2010 , 2011a ).

The logs inhabited by Cryptocercus degrade relatively slowly, conferring a degree of nest stability that allows for the lengthy brood care, frequent physical contact, and behavioural interactions that characterise its social environment (Klass et al., 2008 ). The social environment, in turn, is known to affect reproduction and development in all cockroaches in which it has been studied (Bell et al., 2007 : Table 8.3; Willis et al., 1958 ; Holbrook & Schal, 1998 ; Uzsak & Schal, 2013 ). Tactile stimulation and short‐range and contact pheromones within cockroach social groups not only serve as behavioural releasers, but also regulate physiological processes (Lihoreau & Rivault, 2008 ; Uzsak et al., 2014 ). The strongest effect is on early developmental stages, where the social environment synchronises molting, modifies behaviour and alters developmental rates and body size (Nalepa & Bandi, 2000 ; Bell et al., 2007 ). Such profound and fundamental physiological consequences of social interaction in cockroaches suggest that it lies at the core of the complex caste system exhibited by their termite relatives; social contact currently plays a powerful role in structuring colony level regulatory processes (Springhetti, 1973 ; Greenberg & Stuart, 1979 ; Brent & Traniello, 2001 ; Brent et al., 2007 ; Watanabe et al., 2014 ).

Subsocial to eusocial

How is the transition from a relatively simple, if specialised, subsociality typical of Cryptocercus to a highly complex eusocial life history made without changing the basic ecological context? A parsimonious scenario is that the behavioural and developmental shifts exhibited by extant incipient termite colonies during their establishment and growth recapitulate the evolutionary transition from subsociality to eusociality in an ancestor (Nalepa, 1988b, 1994; Roisin, 1994; Higashi et al., 2000). In young termite colonies, the adults prepare the nest and execute all brood care duties for the eggs and young; oviposition is reduced or suspended during that initial subsocial stage (Weesner, 1960; Nutting, 1969; Shellman‐Reeve, 1997). As colony ontogeny proceeds, brood care responsibilities, including trophallactic feeding of neonates, are assumed by the first offspring to reach the third instar (e.g. Rosengaus & Traniello, 1993); reproductive and developmental trade‐offs simultaneously become apparent. These first alloparents begin undergoing stationary and regressive molts, and the female parent resumes or increases oviposition (Noirot, 1982, 1989; Noirot & Pasteels, 1987). Cooperative breeding via juveniles feeding and tending their younger siblings allows the female parent to devote her nitrogenous resources to egg production while simultaneously imposing a developmental cost on alloparents. This transition scenario is not only fully compatible with cockroach physiology in a nitrogen‐limited environment (Nalepa, 1994, 2011a), but also allows for the increase in colony size that subsequently favours the appearance of a dependent, sterile, defensive caste (Higashi et al., 2000; Nalepa, 2011a). Behavioural changes can be powerful forces in the social and nutritional environments, with evolutionary outcomes easily acquiring a runaway property (Crespi, 2004; Bateson, 2014). An evolutionary cascade precipitated by the onset of alloparental care in the termite ancestor can result in not only a morphologically distinct soldier caste, but also in life history characters specific to termites, including a small body size, fragile morphotype, and extreme phenotypic plasticity (Fig. 2). The latter life history changes were possible because the altricial morphotype of alloparents was made visible to selection when these young helpers became developmentally stalled in an early ontogenetic stage (reviewed by Nalepa, 2011a,b).

Figure 2 Open in figure viewer PowerPoint Transition to eusociality via alloparental care. (a) and (b) as in Fig. 1 ; (c) cooperative breeding was an evolutionarily transient stage still evident during colony foundation in extant one‐piece termites; (d) derived, downstream effects of the initial switch from parental to alloparental care. It is assumed here that alternate developmental pathways ending in a terminal, dependent morphotype (soldiers, neotenic reproductives) are derived because they not only deviate from straightforward, cockroach‐like development, but are contingent on the alloparental behaviour of their siblings.

A third level of dependence One of the most potent evolutionary aftermaths of a transition to alloparental care was the effect it had on the microbial environment within the hindgut. In Cryptocercus, nymphs with an established gut microbiota retain their protists through ecdysis because encystment cycles of the flagellates are exquisitely tuned to the shifting hormonal titres of the host during this time; some protists begin responding to rising levels of ecdysone as much as 50 days prior to host molt (Cleveland & Nutting, 1955; Cleveland, 1957; Cleveland & Burke, 1960). These resistant stages of the protists are then held within the retained cuticular lining of the hindgut during the molting period; afterwards they repopulate the gut of the individual (Cleveland et al., 1934). The inevitable hormonal changes that accompanied developmental shifts in young alloparents, then, would have had an additional and powerful functional consequence: the death of gut protists during the host molting cycle (reviewed by Nalepa, 1994). Although termites have the best studied of the insect gut mutualisms (Engel & Moran, 2013), the loss of the large, cellulolytic gut protists during the molting cycle in lower termites continues to be misunderstood (e.g. Troyer, 1984; Thorne, 1997; Korb, 2009). These symbionts are not ‘shed’, ‘discarded’ or ‘cast’ with the hindgut lining; the protists are dead and gone from the hindgut prior to the molt of their host (Cleveland, 1925, 1965; Andrew, 1930; Grassé, 1952; Nutting, 1956; Cleveland & Burke, 1960; To et al., 1980). The gut is empty 7 days before molt in Kalotermes flavicollis (Fab.) (Lüscher, 1960) and 6 days before molt in Coptotermes formosanus (Shiraki) (Raina et al., 2008). As in Cryptocercus, the lining of the hindgut is retained within the body during ecdysis; it later breaks up and is excreted (Cleveland et al., 1934; Grassé & Noirot, 1945). Consequently, the gut protists cannot be re‐acquired by a post‐molt termite via (i) feeding on its own shed exuvium, (ii) that of a nestmate, or (iii) feeding on faeces. The sole mechanism of refaunation in a newly molted termite is via repeated proctodeal trophallaxis. The small polymastigotes become re‐established within 3 or 4 days after ecdysis, but it can take up to 2 weeks for complete refaunation (Nutting, 1956). This is in stark contrast to the ancestral relationship to symbionts as typified by Cryptocercus, and likely derived from the physiological basis of the monumental shifts in development exhibited by extant OP termites in relation to their cockroach ancestors: stasis in an altricial morphotype, and the extraordinary phenotypic plasticity of their developmental trajectory. The idea is supported by a lifetime of work by L.R. Cleveland, who demonstrated the extreme vulnerability of gut protists to the titre and/or timing of host hormonal surges during molt in both Cryptocercus and termites. The idea also accords with the axiom that changes in insect life history strategies are proximately rooted in alteration of the timing or action of the hormones that integrate nutritional status with developmental timing (Spicer & Burggren, 2003; Erezyilmaz, 2011; Johnson et al., 2014).

Consequences Alloparental care, then, precipitated a new, third level of dependence. The termite ancestor: (i) relied on hindgut symbionts to metabolise and supplement a wood diet; (ii) had altricial neonates that relied on their parents for food, protection and symbionts; and now (iii) all non‐terminal developmental stages of the family depend on each other for the restoration of gut symbionts after molting. The periodic loss of symbionts removes the option of living independently because it mandates access to the hindgut fluids of a nestmate (Nalepa, 1994). Whereas all offspring in the family of a subsocial ancestor were capable of independence and eventual reproduction after the third instar, they could replicate only as part of the larger social group after alloparental care was initiated. Fixation of eusociality quickly followed. Individuals could not defect, nor could the newly eusocial family revert to a previous state. They had become a physiological unit, and death became inevitable for an individual separated from the colony (Eggleton, 2011). Evolutionary interests became aligned, with saltation in the hierarchical level at which natural selection operated. Individuals that had been potentially autonomous after the third instar became a dependent, integrated part of a higher level whole: the very definition of a major evolutionary transition (Maynard Smith & Szathmáry, 1995). Little response of the gut microbial community was required when their hosts became interdependent, as the behaviour of alloparents assured inter‐host continuity (Nutting, 1956). Alloparental proctodeal trophallaxis, originally extended to younger siblings, simply became extended to all other family members. Instead of host‐symbiont fitness, colony‐symbiont fitness became coupled, with intermolt termites serving as reservoirs. In extant termite colonies, protist numbers are dynamic, and rise, fall or disappear in the gut with colony ontogeny and the function and developmental stage of individual colony members (e.g. Shimada et al., 2013).