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This article was originally published in the Encyclopedia of Animal Behavior published by Elsevier, and the attached copy is provided by Elsevier for the author's benefit and for the benefit of the author's institution, for non- commercial research and educational use including without limitation use in instruction at your institution, sending it to specific colleagues who you know, and providing a copy to your institution’s administrator. All other uses, reproduction and distribution, including without limitation commercial reprints, selling or licensing copies or access, or posting on open internet sites, your personal or institution’s website or repository, are prohibited. For exceptions, permission may be sought for such use through Elsevier's permissions site at: http://www.elsevier.com/locate/permissionusematerial Duffy J.E. (2010) Crustacean Social Evolution. In: Breed M.D. and Moore J., (eds.) Encyclopedia of Animal Behavior, volume 1, pp. 421-429 Oxford: Academic Press. © 2010 Elsevier Ltd. All rights reserved. Author's personal copy Crustacean Social Evolution J. E. Duffy, Virginia Institute of Marine Science, Gloucester Point, VA, USA ã 2010 Elsevier Ltd. All rights reserved. Introduction shed periodically during growth. Each of the segments in the primitive ancestral crustacean body bore a pair of The Crustacea represent one of the most spectacular appendages, which have been modified during the evolu- evolutionary radiations in the animal kingdom, whether tion of the various crustacean groups into a wide range of measured by species richness or diversity in morphology structures used in feeding, locomotion, sensation, and or lifestyles. Its members range from microscopic mites of communication. The bodies of most crustaceans are the plankton to fearsome giant crabs to sessile barnacles to richly endowed with a wide variety of setae – stiff hair- amorphous parasites that are almost unrecognizable as like bristles of diverse form that are used for a wide range animals. Crustaceans occupy most habitats on earth, of functions. The two pairs of antennae, in particular, bear from the deepest ocean trenches to mountaintops and dense arrays of chemo- and mechanosensory setae, which deserts, and the dominance of the open ocean plankton are used in conjunction with directional currents of water by calanoid copepods makes them one of the most abun- generated by specialized appendages in the head region to dant metazoan groups on earth. distribute and collect chemical signals, and are important This ecological diversity suggests that the Crustacea in social and mating interactions. should provide a wealth of interesting social and mating The mode of development strongly influences the systems, and this is indeed true, as both classic and recent potential for kin to interact, and thus the evolution of research has shown. Yet, despite their ubiquity and diver- social systems in Crustacea. Most familiar decapods sity, crustaceans have received surprisingly little attention release microscopic larvae into the plankton, where they from students of behavior compared with their younger drift for some time – several months in some species – siblings – the insects – or the vertebrates, no doubt due in before settling to the bottom and transitioning to the adult large part to the aquatic habits of most crustacean species. lifestyle. In such species, populations are genetically well What are the ecological and behavioral consequences of mixed and kin groups cannot form. In other species, the crustacean colonization of this range of habitats? What however, eggs hatch directly into miniature versions of can they tell us about the generality of theory and the the adults in much the same way as eggs hatch into generalizations emerging from work on other, better stud- miniature adults (nymphs) in hemimetabolous insects ied taxa? Here, I highlight a few illustrative case studies of such as grasshoppers and termites. This direct develop- social systems in crustaceans, and discuss the broader ment is common to all peracarid crustaceans (isopods, implications of crustacean sociality for understanding amphipods, and their relatives) and is also found in some some central issues in animal behavior and sociobiology. decapods. Crustaceans go through several molts as they grow, before reaching the adult stage. Crustaceans display a wide range in reproductive biol- A Primer in Crustacean Biology ogies. While most species breed repeatedly during life and have separate sexes, brine shrimp and some Daphnia that Recent research in molecular systematics shows that the inhabit temporary freshwater pools are cyclic partheno- Crustacea is paraphyletic, with the insects (Hexapoda) gens, and several shrimp are sequential or simultaneous nested within a pancrustacean clade that diverged in the hermaphrodites. Sex determination can be genetic, envi- Precambrian. Among the major branches in the crusta- ronmental, or involve some combination of the two. cean family tree, the Malacostraca is the most diverse, both in morphology and in species, numbering tens of thousands. This group includes the large, ecologically Crustacean Mating Systems and economically important crabs, shrimps, and lobsters The mating system is an important component of the familiar to the layperson. For all of these reasons, most of what is known about the social behavior of crustaceans social system in that it influences the size, composition, comes from the Malacostraca. and kin structure of groups of interacting individuals. For Like their relatives, the insects, crustaceans share a example, establishment of monogamous relationships can basic segmented body plan divided into three regions: lead to paternal care, and in some animals, avoidance of the head, thorax (pereon), and abdomen (pleon). The incest helps explain why adult helpers in social colonies body is covered with a chitinous exoskeleton, which is do not breed. Crustaceans display a wide diversity of 421 Encyclopedia of Animal Behavior (2010), vol. 1, pp. 421-429 Author's personal copy 422 Crustacean Social Evolution mating systems that are molded by the variance in mate Males often do not feed while guarding so they incur a availability in time and space, variation in female life cost in exchange for the opportunity to mate. Females history, and behavior. These range from situations involv- presumably also incur a cost in terms of reduced feeding, ing fleeting encounters to various forms of mate guarding, higher predation risk, and/or increased risk of being dis- monogamous pair formation, to harems. Here, I describe a lodged from the substratum. Indeed, experiments with the few examples that provide insights into the evolution of isopod Idotea baltica, conducted by Veijo Jormalainen and more advanced social systems. colleagues, showed that guarded females had lower gly- cogen (stored food) reserves and laid smaller eggs than females that had been mated but not guarded. Not sur- Precopulatory Mate Guarding and Its prisingly, female isopods often vigorously resist being Consequences guarded and the initiation of guarding tends to be a mutu- ally aggressive affair. The proposed role of limited recep- A key trait influencing the mating system in many crus- taceans is the limited time window of female receptivity, tivity in selecting for mate guarding would seem to be which results from the requirement that mating and ovu- proved by the exception to the rule: in terrestrial oniscoid isopods, females have extended receptivity and some can lation take place immediately after a molt when her integument is soft. As a consequence, many crustaceans store sperm – using it for up to eight broods, reducing a exhibit mate guarding, pair-bonding, and other behaviors male’s ability to monopolize mating opportunities. Accord- ingly, these isopods lack prolonged guarding. that maximize a male’s certainty of having access to a female when she is ready to mate. Precopulatory mate Sexual selection has molded the phenotypes of such guarding (also called amplexus), in which the male carries mate-guarding species. Males are larger than females in the female for an extended period of time in anticipation several mate-guarding isopods, likely because larger male size is favored by both intrasexual selection, which favors of mating, is common in several groups of amphipods, including the familiar Hyalella species of North American larger size in competition among males, as well as intersex- lakes and Gammarus species of coastal marine waters, as ual selection generated by females resistant to guarding. Strong sexual dimorphism is also seen in some freshwater well as many groups of isopods (Figure 1). Because of brief female receptivity, the operational sex ratio in such amphipods. Interestingly, among closely related species of populations is highly male-biased, and this mate guarding the amphipod Hyalella, the dimorphism is reduced in species that inhabit lakes with fish, which impose strong size- allows the male to monopolize the female until she is receptive. In other species, including several crabs and selective predation on large individuals; in these popula- lobsters, females can store sperm and so are not tempo- tions exposed to predation, moreover, females show weaker rally restricted in mating time. preference for large males. Thus, phenotypic traits and behavioral preferences are molded by the trade-off between Mate guarding has been extensively studied in isopods and amphipods as a model system for understanding sexual selection for large

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