Synalpheus regalis is a shrimp that commonly live in sponges of coral reefs along the tropical West Atlantic. These snapping shrimps form a prominent component of the diverse cryptofauna. For the span of their entire lives, these shrimp live in the internal canals of the host sponge, using it as a food resource and shelter. It has been shown that colonies contain over 300 individuals, but only one reproductive female. Also, larger colony members, most of which apparently never breed, defend the colony against heterospecific intruders. This evidence points towards the first case of eusociality in a marine animal.
Behavior and ecology
J. Emmett Duffy, a primary investigator of S. regalis, uses the term "eusociality" to refer to the syndrome of multigenerational, cooperative colonies with strong reproductive skew (usually a single breeding female) and cooperative defense of the host sponge found in several Synalpheus species. Eusociality requires that generations overlap, allowing close contact between individuals such that altruistic behaviors can be favored by kin selection. The populations that live in sponges contain a few hundred individuals, each with two generations of kin. Also, by having just one reproductive female, colonies clearly fit the first criterion of reproductive division of labor. Most hypotheses that explain eusociality entail some form of adaptive division of labor, which results in enhanced reproductive output of the breeders and inclusive fitness benefits for the nonbreeding helpers.
Fortress defense is one of two modes of eusociality. Queller and Strassmann (1998) distinguished between "life insurers", which include most Hymenoptera, where cooperation reduces the risk of total reproductive failure, and "fortress defenders", where cooperation enhances the defense of a commonly held, valuable resource.
Crespi (1994) argued that three conditions must be met to explain most cases of fortress defense: a coincidence of food and shelter in an enclosed habitat, a high value of food-habitat resources that renders inhabitants vulnerable to predatory attacks, and the ability to defend the resource effectively. The strong selective pressures of enemies on kin-structured aggregations may promote evolution of specialized defenders that raise their own and the breeders' inclusive fitness by defending the colony. Because few predators can enter the narrow canals of the sponges, the greatest competition comes from enemies that are of the same or closely related species.
S. regalis lives and feeds exclusively within their hosts, therefore meeting the first condition. Also, data shows that fewer than 5% of sponges sampled were unoccupied by shrimp, which means that sponges are in short supply and subject to strong competition. Finally, the large non-breeding defenders utilize the snapping claw, a potent weapon that produces a water jet intense enough to stun small animals. S. regalis appears to reach Crespi's (1994) three criteria.
A study was conducted to observe the responses of colonies by introducing heterospecific intruders. The results were dramatic: contact between a resident and an intruder generally resulted in an intense battle, with both individuals snapping at each other with their powerful major chelae. However, contacts between residents and 'natives' were quite peaceful. The larger residents were the most active and aggressive, contacting foreign intruders more than twice as often as did smaller residents, and engaging intruders in combat (snapping) ten times more often than did juveniles. The larger shrimp tend to be older than the rest of the colony, and thus they allocate their energy to defending rather than breeding. Such size- or age-related polyethism is a common aspect of labor specialization among social insects. Since most of the defenders do not breed, the only way to secure their genes in future generations is to protect their juvenile siblings, allowing them to grow to adulthood free from predation and survive long enough to reproduce. This nest defense amounts to cooperative brood care and establishes S. regalis as a eusocial species.
If fortress defense plays an important role in favoring cooperation among sponge-dwelling shrimps, it can be predicted that eusociality would enhance the ability to acquire, defend, and retain limited host resources compared to less social species. Duffy and Macdonald (2010) tested this prediction in Belize by examining how shrimp abundance correlated with sociality among species. They discovered that eusocial species are more abundant, occupy more sponges and have broader host ranges than non-social sister species.
S. regalis are exceptionally tolerant of conspecifics within their colonies, and aggressive towards conspecifics not of their own colony. These peaceful interactions are attributable to close genetic relatedness among nestmates. Allozyme data revealed that relatedness within colonies is high, averaging 0.50, indicating that colonies in this species represent close kin groups. The existence of such groups is an important prerequisite of explanations of social evolution based on kin selection. During the intruder experiment, resident shrimp contacted foreign conspecifics less and snapped more frequently than they did when faced with a nestmate. Because nestmates are generally close kin in S. regalis, this discrimination may reflect kin recognition and may help maintain the integrity of kin-structured social colonies.
Nestmate discrimination likely involves both waterborne and contact chemical signals which have been shown to mediate sex recognition in other alpheids. The high frequency of intruder contacts with the queen may suggest that she produces pheromones like in social insects.
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