Social biology of the wood-feeding cockroach genus Salganea (Dictyoptera, Blaberidae, Panesthiinae): did ovoviviparity prevent the evolution of eusociality in the lineage?

Maekawa, Kazuyuki; Matsumoto, Tadao; Nalepa, Christine A.

doi:10.1007/s00040-008-0997-2

Cited by 34 publications

(35 citation statements)

References 37 publications

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“…It was no doubt a complex, hierarchical process dependent on a suite of interrelated life history characters including oviparity, multiple symbiotic relationships, progressive provisioning, hatching asynchrony, long-lived adults, and semelparity (Klass et al 2008;Maekawa et al 2008;Nalepa 1988Nalepa et al 2001a;Bell et al 2007). A crucial character, and one not previously examined in this context, is body size.…”

Section: The Ancestormentioning

confidence: 96%

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Body Size and Termite Evolution

Nalepa

2011

Evol Biol

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Termites are a monophyletic lineage within the paraphyletic Blattaria, with xylophagous cockroaches in the genus Cryptocercus as sister group. Given this ancestry, termite divergence involved a substantial leap in body plans, as they are pale, fragile, and miniaturized relative to most cockroaches. Here I suggest that the evolutionary transition to an altricial morphotype in termites is grounded in the economics of utilizing a wood diet, and occurred via a series of sequential steps associated with modifications in social behavior. The chief benefit of an altricial morphotype is suggested to be nitrogen made available by decreasing individual body size and by dispensing with a heavy, melanized cuticle. The primary costs lie in increased vulnerability to environment hazards, including predators, pathogens, and desiccation. Termites tipped the evolutionary scale via cooperative behaviors that mitigate the cost or amplify the benefit of a small, fragile morphotype, and were present in rudimentary form in their cockroach relatives. These include building behavior, cooperative feeding, allogrooming, and most notably, trophallaxis. It was the directed circulation of nitrogenous reserves via trophallactic feeding among units of the superorganism rather than their progressive storage in a large, heavily armored body that was the foundation of termite evolutionary success.

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Section: The Ancestormentioning

confidence: 96%

“…It is not a direct ancestor to descendant comparison, but given the convergence of morphology, behavior and life history in even distantly related wood feeding cockroaches (Bell et al 2007;Maekawa et al 2008), we can predict with a fair amount of confidence some key biological and life history characteristics of the termite ancestor.…”

Section: The Ancestormentioning

confidence: 98%

Body Size and Termite Evolution

Nalepa

2011

Evol Biol

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“…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, ); 4–6 years in Panesthia cribrata Saussure (Rugg & Rose, ); and up to 7 years in Cryptocercus clevelandi Byers (Nalepa et al, ). 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.…”

Section: The Ancestral Life Historymentioning

confidence: 99%

Origin of termite eusociality: trophallaxis integrates the social, nutritional, and microbial environments

Nalepa

2015

Ecological Entomology

138

163

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Abstract. 1. Numerous cladistic analyses have converged: termites are a monophyletic clade embedded within the paraphyletic cockroaches, and sister group to the biparental, wood-feeding cockroach Cryptocercus. The latter is, therefore, an appropriate model for testing assumptions regarding early termite evolution.2. The ground plan of the termite ancestor is reviewed based on shared characters of ecology, life history, and behaviour in Cryptocercus and incipient termite colonies, and includes two levels of dependence: a reliance of all individuals on gut microbiota, and dependence of early instars on parental care. Both these conditions co-evolved with parent-to-offspring proctodeal trophallaxis.3. The termite ancestor lived in a single log serving as food and nest. This 'one-piece' nesting ecology prioritises nitrogen conservation and strongly influences interacting social, nutritional, and microbial environments. Each of these environments individually and in combination profoundly affect cockroach development.4. Proctodeal trophallaxis integrates the social, nutritional, and microbial environments. A change in trophallactic behaviour, from parental to alloparental, can, therefore, shift developmental trajectories, ultimately adding a third level of dependence. The death of gut protists during the host molting period and consequent interdependence of family members shifted the hierarchical level at which selection acted; fixation of eusociality quickly followed.5. The basic nesting ecology did not change when termites evolved eusociality, the change occurred in the allocation and use of existing resources within the social group, driven by nitrogen scarcity, mediated by trophallaxis, and made possible by a strongly lineage-specific set of life history characteristics.

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“…In wood‐feeding cockroaches, parental feeding behaviors have been reported in two subsocial genera, Cryptocercus Scudder (Cryptocercidae) and Salganea Stål (Blaberidae: Panesthiinae) (Nalepa et al . 2001; Maekawa et al . 2008).…”

Section: Introductionmentioning

confidence: 99%

“…The gut microbes of Panesthiinae including Salganea resemble those of non wood‐feeding cockroaches (Kidder 1936; Bell et al . 2007), but stomodeal (oral) trophallaxis, in which young nymphs cling to the mouthparts of parents and appear to take liquids by stomodeal feeding, has been observed in Salganea taiwanensis Roth (Maekawa et al . 2008).…”

Section: Introductionmentioning

confidence: 99%

Description of the basic features of parent-offspring stomodeal trophallaxis in the subsocial wood-feeding cockroach Salganea esakii (Dictyoptera, Blaberidae, Panesthiinae)

Shimada

Maekawa

2010

Entomological Science

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In subsocial xylophagous cockroaches it is thought that parental feeding is important for the survival and growth of the altricial offspring, but the details of parental feeding in these groups are poorly known. We observed stomodeal (oral) trophallaxis between parents and the 2nd or 3rd instars of the wood-feeding cockroach Salganea esakii Roth, and here report basic features of trophallaxis in young families. Both the female and male parents fed young nymphs with stomodeal food, and there was no difference in the frequency of the behavior between parental sexes. Up to three nymphs could be fed simultaneously during a single trophallactic event. Adults occasionally rejected contact with nymphs by blocking them with their forelegs. Nymphs utilized trophallactic food from parents more frequently than feeding independently on wood pieces or fecal pellets. Trophallaxis between sibling nymphs was never observed. These results suggest that the 2nd and 3rd instar nymphs rely on the stomodeal substances provided by their parents, and that provisioning is an essential component of subsocial behavior in biparental wood-feeding cockroaches.

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Social biology of the wood-feeding cockroach genus Salganea (Dictyoptera, Blaberidae, Panesthiinae): did ovoviviparity prevent the evolution of eusociality in the lineage?

Cited by 34 publications

References 37 publications

Body Size and Termite Evolution

Body Size and Termite Evolution

Origin of termite eusociality: trophallaxis integrates the social, nutritional, and microbial environments

Description of the basic features of parent-offspring stomodeal trophallaxis in the subsocial wood-feeding cockroach Salganea esakii (Dictyoptera, Blaberidae, Panesthiinae)

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