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, 100 (22), 12808-13

Evolution of Eusociality and the Soldier Caste in Termites: Influence of Intraspecific Competition and Accelerated Inheritance

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Evolution of Eusociality and the Soldier Caste in Termites: Influence of Intraspecific Competition and Accelerated Inheritance

Barbara L Thorne et al. Proc Natl Acad Sci U S A.

Abstract

We present new hypotheses and report experimental evidence for powerful selective forces impelling the evolution of both eusociality and the soldier caste in termites. Termite ancestors likely had a nesting and developmental life history similar to that of the living family Termopsidae, in which foraging does not occur outside the host wood, and nonsoldier helpers retain lifelong options for differentiation into reproductives. A local neighborhood of families that live exclusively within a limited resource results in interactions between conspecific colonies, high mortality of founding reproductives, and opportunities for accelerated inheritance of the nest and population by offspring that differentiate into nondispersing neotenic reproductives. In addition, fertile reproductive soldiers, a type of neotenic previously considered rare and docile, frequently develop in this intraspecific competitive context. They can be highly aggressive in subsequent interactions, supporting the hypothesis that intercolonial battles influenced the evolution of modern sterile termite soldier weaponry and behaviors.

Figures

Fig. 1.
Fig. 1.
Natural chambers of young Zootermopsis colonies revealed under the bark of a Ponderosa pine tree; note close proximity of neighboring families and therefore high probability of interactions in the field.
Fig. 2.
Fig. 2.
Occurrence of secondary reproductives in control vs. interaction colonies. Normal neotenic (a), reproductive soldier (soldier neotenic) (b), and secondary reproductives (neotenics and/or reproductive soldiers) (c) differentiate significantly more frequently after intercolony interactions than in control colonies (and only in controls in which founding reproductives died). Compare columns with the same letters; if case differs, they are significantly different. χ2 levels of significance: Aa, P < 0.0001; Bb, P < 0.0001; Cc, P < 0.05; Dd, P < 0.0001.
Fig. 3.
Fig. 3.
Time spent in nursery area of the nest by normal soldiers and reproductives. Normal soldiers rarely associate with eggs and dependent brood in the nursery; in this regard, reproductive soldiers behave like other reproductives. Compare columns with the same letters; if case differs, they are significantly different (χ2 analysis; P < 0.0001).
Fig. 4.
Fig. 4.
Differential targeting of castes by reproductive soldiers vs. normal soldiers. (a and b) Castes and polyphenism within colonies. Number indicates caste: 1, queen; 2, reproductive soldier; 3, normal soldier; 4, alate; 5, nymph; and 6, worker. (c) mRSs selectively attack other male reproductives during intercolony interactions (treatments I and II combined, thus categories are context-dependent and proportions do not add to 100). χ2 levels of significance: Aa, P < 0.001; Bb, P < 0.0001; Cc, not significant; Dd, no attacks by normal soldiers on female neotenics; Ee, P < 0.0001; Ff, P < 0.05. Compare columns with the same letters; if case differs, they are significantly different (P ≤ 0.05).

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