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Review Article Indian Journal of Geo Marine Sciences Vol. 46 (08), August 2017, pp. 1511-1518 Review article Emergence of eusociality in aquatic environment: Synalpheid shrimps show the way! T. Subramoniam Centre for Climate Change Studies, Sathyabama University, Jeppiaar Nagar, Rajiv Gandhi Salai, Chennai – 600119. Tamil Nadu. India [Email: [email protected] ] Received 16 April 2015 ; revised 22 November 2016 Life history traits such as direct development and restricted dispersal, ecological specialization to live in the host sponge, defending the valuable host resource, as well as selective breeding by one or more queens contribute to the evolution of eusociality in marine Crustacea, in particular, the synalpheid shrimp. This review critically examines the preconditions necessary for the evolution of complex social behaviours and structures including eusociality in these symbiotic shrimps and other crustacean species. [Key words: Eusociality, mating systems, coral reef crustaceans, synalpheid shrimps, communal living] Introduction Eusociality, the apex of animal social searching” to complex social monogamy with organization is defined by Wilson1 as the mate guarding practises, along with their condition of multiple generations organising into symbiotic mode of living with other marine groups by means of an altruistic division of invertebrate species, may be the harbinger of labour. The condition extends further into communal living and the evolutionary origin of cooperative care of offspring, and reproductive eusociality. The social Synapheus shrimps are skew, by which reproduction is relegated to a generally monogamous carideans, living as single mother queen. Such advanced social symbionts inside the marine sponges, life-long, systems have been well recognised only among and produce crawling larvae that are retained in social insects and the African mole-rats2. Among the sponge colony, across generations4. The the aquatic organisms, crustaceans have the resulting kinship relationship among the offspring unique distinction of having evolved such plays a pivotal role in the progression towards complex social systems only in the coral reef- social behaviour, ultimately leading to associated caridean shrimps. Various sponge- eusociality. In addition, prolonged parental care dwelling snapping shrimp species, composing the of the young in a microhabitat has also bolstered taxonomic family Synalpheus, developed well- social living and near-eusocial conditions in coordinated aggregations, which may seem to be certain crabs and peracarides5. This review on the cusp of eusociality. Sexual patterns and endeavours to analyse various preconditions that modes of development are the most important life promote evolutionary origin of social systems, history traits in the coral reef associated caridean which qualify crustacean species such as shrimps3. However, it is the diversified mating Synalpheid shrimps to eusocial conditions, strategies ranging from promiscuous “pure among aquatic organisms. 1512 INDIAN J. MAR. SCI., VOL. 46, NO. 08, AUGUST 2017 Social insects eusociality has evolved in mole-rats through kin Eusocial behaviour of social insects mainly selection and in response to constraints imposed depends on the ability of the group members to by ecological factors such as distribution of food develop different castes with their respective in the form of underground roots and tubers. By division of labour. As an example, the honeybees living in large social groups with cooperation and live in highly structured colonies. Reproduction is reproductive repression, eusocial mole-rats are by the queen and drones, and the infertile able to exploit an ecological niche where solitary females, the workers, perform all other duties to animals or small groups would be unlikely to support the colony. The young workers tend the survive. Incidentally, members of the burrowing larvae, and then switch functions to forage and rodent family, Bathyergidae, to which the mole- collect pollen or nectar6. Honeybee vitellogenin, rats also belong, exhibit varied social strategies besides its principal role of providing precursors that include solitary, social/colonial dwelling, to yolk formation, exerts an effect on division of and, at the extreme, the eusocial condition as seen labour, and reduces oxidative stress by in the mole-rat Heterocephalus glaber8. scavenging free radicals, thereby prolonging Correlatively, the caridean alpheid shrimps also lifespan in the facultative sterile workers and the represent a single taxonomic group in which an reproductive queen6. Sterile workers (genetic entire spectrum of sociality is witnessed; with females) are capable of synthesizing vitellogenin, only sponge-dwelling synalpheids evolving into a but use it only for making the royal jelly to feed eusocial condition (see below). the larvae. Understandably, the social life history traits of hymenopteran insects are determined by Synalpheid shrimps vitellogenin, which in insects is synthesized under Recognition of eusociality in the control of juvenile hormone7. It can therefore crustaceans inhabiting the aquatic environment be presumed that this hormone could be the is rather recent with the lifestyle description of ultimate decider of caste differentiation in these sponge-dwelling alpheid shrimp species, eusocial insects. belonging to the genus Synalpheus9. These coral-reef dwelling caridean shrimps have African naked mole-rats adapted to these specialized niches, on which In another example, the extremely eusocial they have depended for both shelter and food. African naked mole-rats characteristically live in Naturally, these symbiotic synalpheid shrimps colonies containing overlapping generations that developed innovations in their social behaviour, cooperate in the rearing of their offspring8. with respect to defending their bio-shelters, as Reproduction is normally monopolized by a well as in life history strategies that will bolster single breeding queen, who mates with one to retention of successive generations in the same three breeding males. All other colony members colony. Since such elaborate and safe sponge either act as “workers”, maintaining the burrow hosts for colonization are hard to find in the system, or “soldiers”, defending the colony crowded coral reef environment, the shrimps against foreign mole-rats or snakes. Although guard their invertebrate hosts fiercely with they have enhanced longevity, they suffer from powerful weaponry such as their snapping chronic infertility and never reproduce. The claws. Arguably, the first step in the evolution of socially induced suppression of reproduction in social behaviour of these shrimps may be the male and female mole rats is mediated by a successful occupation and defence of their mechanism involving direct contact with the symbiotic invertebrate hosts. breeding queen, rather than by primer Furthermore, many of the marine shrimp pheromones. Subtle agonistic interactions belonging to the genus Synalpheus exhibit social between the queen and non-breeders cause a monogamy, in which adults live as heterosexual neuroendocrine response in the latter, the pairs in a burrow (Table 1). Since female physiological result of which is inhibition of receptivity is restricted to a brief period after gonadal function and infertility. The genetic moulting, as in many decapods, males practise relatedness is very high in these eusocial forms, precopulatory mate-guarding and do not allow due to high inbreeding and the absence of other males into their territory. Social dispersal of non-breeders. It is thought that monogamy in these pair-forming alpheids is also SUBRAMONIAM: EMERGENCE OF EUSOCIALITY IN AQUATIC ENVIRONMENT 1513 maintained by cooperative defending of the entire reproduction is carried out by the termite common burrow by the pair10. A more complex queen in a colony, thereby making a level of communal living is found in some resemblance between the social insects sponge-dwelling synalpheid species such as (termites) and the synalphid social shrimps. Synalpheus longicarpus, in which hundreds of Evidently, social monogamy seems to be the heterosexual pairs cohabit in a host with forerunner of eusociality in the sponge-dwelling multiple breeding females11. A further road to Synapheus shrimp for the reason that there is eusociality is however witnessed in certain direct development (bypassing planktonic species such as S. regalis, S. filidigitus, and S. dispersive larval stages) and a long-term parent- rathbunae (Table 1). All these fully eusocial offspring association which fosters formation of species live in colonies of hundreds of close kin groups. Thus, in these caridean individuals inside the spongocoel, with only a shrimps, the defining eusocial characteristics single female, breeding, as in S. regalis. In include (1) symbiotic social living in sponges another eusocial species, S. chacei, the colonies which provides shelter and food, (2) mate- are much smaller, but genetically heterogeneous. guarding and shared resource defence, (3) non- This genetic heterogeneity in S. chacei is due to dispersive larvae, and (4) social monogamy. In the presence of multiple queens in the colony. the eusocial species such as S. regalis, there is a The females of this multi-queen colonies are not strong reproductive skew, brought about by only smaller, but also possess the snapping restriction of reproduction to a single queen and claws12. As suggested by Duffy4 this condition a few male partners11. In addition, genetic may enhance
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