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This Article Was Originally Published in the Encyclopedia of Animal 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 Grosberg R. and Plachetzki D. (2010) Marine Invertebrates: Genetics of Colony Recognition. In: Breed M.D. and Moore J., (eds.) Encyclopedia of Animal Behavior, volume 2, pp. 381-388 Oxford: Academic Press. © 2010 Elsevier Ltd. All rights reserved. Author's personal copy Marine Invertebrates: Genetics of Colony Recognition R. Grosberg and D. Plachetzki, University of California, Davis, CA, USA ã 2010 Elsevier Ltd. All rights reserved. Introduction with respect to the genetic identities of interactors; (2) genetically based recognition cues govern the expression Many sessile, encrusting clonal and colonial marine of these behaviors; and (3) the diversity of these cues is built animals – notably sponges, cnidarians, bryozoans, and on unusually high levels of genetic variation. colonial ascidians – exhibit a suite of life-history traits In this way, several features of invertebrate allorecogni- that promote intraspecific competition for space and the tion systems mirror several aspects of the major histocompat- evolution of complex behaviors that mediate the out- ibility complex (MHC), a key element of the vertebrate comes of somatic interactions. These traits include the adaptive immune system. For this reason, analogies between capacity for indeterminate growth and reproduction, often the vertebrate immune system and invertebrate allorecog- augmented by limited dispersal and, in some cases, kin- nition behavior inspired many early studies of invertebrate directed settlement behavior of their sexual and asexual allorecognition, with the hope of discovering retained propagules . In these taxa, intraspecific competitive interac- ancestral features of our own MHC. We now understand tions elicit behaviors ranging from no apparent response, that most of the similarities between invertebrate allore- through active cytotoxic rejection, to intergenotypic cognition and vertebrate MHC systems are superficial and fusion of individuals and colonies. Among cnidarians likely reflect convergent evolution, not common ancestry. and some bryozoans, incompatibility responses extend Still, these parallels may reveal common selective forces beyond simple rejection, often eliciting a complex suite that have led to the evolution of the diverse array of of agonistic behaviors. In addition, developmental transi- allorecognition systems, including the vertebrate MHC. tions in the expression of these complex fusion and rejec- For instance, the function of both allorecognition and the tion behaviors may also occur. MHC relies on extremely high levels of genetic polymor- As in many social insects and vertebrates that modify phism that confer cue specificity. The use of highly poly- the expression of their social behaviors according to the morphic, genetically based phenotypic cues to regulate the relatedness of conspecifics, a growing number of field and expression of these social behaviors (including inbreeding laboratory studies on colonial marine invertebrates show avoidance) and immune function potentially imposes that neither intergenotypic rejection and aggression, nor selection on the genes that produce these cues. fusion randomly occur with respect to the genotypes of Understanding how natural selection influences the interacting conspecifics. Instead, the initiation of agonistic evolution of this exacting specificity and its underlying behavior often depends on the relatedness of contestants: genetic diversity fundamentally requires an integrated interactions between clonemates and close kin generally analysis of both formal and molecular genetics of allor- do not elicit cytotoxicity or aggression, whereas interac- ecognition. Formal genetic approaches generally involve tions between more distant relatives do. Likewise, somatic breeding animals with different phenotypes, and then fusion usually occurs only between clonemates and close correlating the phenotypes of progeny with the presence kin. Thus, precise allorecognition, the ability to distin- or absence of genetic markers over successive crosses. In guish self from conspecific nonself, once thought to be the so doing, breeding studies can circumscribe how many hallmark of the vertebrate immune system, is phyletically loci are involved in the trait (i.e., how many distinct broadly distributed, and appears to be a ubiquitous feature markers correlate with the allorecognition phenotype), of all multicellular animals, along with fungi, myxobac- the degree to which certain alleles are dominant over teria, and myxomycetes. others in the expression of a given allorecognition pheno- Pioneering studies of invertebrate allorecognition, dat- type, and the level of standing genetic variation that exists ing back a century to classic studies on the colonial in a given population for an allorecognition phenotype ascidian Botryllus schlosseri, made it clear that specificity (i.e., how many allorecognition classes, or allotypes, segre- in the expression of intercolony fusion and rejection was gate in a population). Alternatively, studies on the molec- heritable. Thus, allorecognition in these taxa provided an ular genetics of allorecognition can reveal the specific early model for the studies of behavioral genetics. The depen- genes involved in these phenotypes and provide primary dence of somatic rejection, aggression, and fusion on relatedness, sequence-level resolution on the identity of loci involved together with discrimination reliabilities that often in allorecognition. Such data make it possible to compare exceed 95%, implies that (1) these behaviors enhance how alleles differ from each other, provide direct mea- individual and inclusive fitness by mediating responses sures of how natural selection acts on individual loci, and 381 Encyclopedia of Animal Behavior (2010), vol. 2, pp. 381-388 Author's personal copy 382 Marine Invertebrates: Genetics of Colony Recognition reveal how specific regions or positions within these loci evolve. In this way, formal and molecular genetic approaches complement each other and together offer powerful tools for deciphering the evolutionary genetics of allorecognition. To this end, two marine invertebrate model systems have emerged over the last two decades, one focusing on the colonial ascidian genus Botryllus (Phylum Chordata), and the other on colonial hydrozoans in the genus Hydrac- tinia (Phylum Cnidaria). In both these cases, formal and molecular genetic approaches have begun to reveal key components of the allorecognition machinery. These components minimally include the genes encoding recep- tors and cues that determine behavioral responses to other conspecifics. Here, we summarize what is presently understood about the genetics of allorecognition in these two taxa, along with the far more limited data that pres- ently exist for bryozoans and sponges. We also evaluate the functional significance of allorecognition in colonial marine invertebrates and consider how various forms of natural selection can explain what is presently understood of the genetics of allorecognition. Finally, we review the Figure 1 Colony structure and ecology of the colonial ascidian broad macroevolutionary patterns of allorecognition behav- ior in colonial invertebrates and consider the factors that Botryllus schlosseri. (a) The adult zooids (the modular, cloned units that compose a colony) of B. schlosseri form star-shaped may have contributed to their evolution. systems embedded in a gelatinous tunic. Numerous tiny saccular ampullae of the tunic’s interzooidal blood-circulatory complex fringe the colony’s complex blood vascular system. (b) A group of Genetics of Allorecognition in Botryllus adult zooids, asexual buds (which sequentially and schlosseri synchronously develop into new zooids), and peripheral finger- like projections of the blood-vascular system called ‘ampullae’ (sites of allorecognition). (c) Competition for spatial resources is The formal and molecular genetics of allorecognition are fierce. Individual colonies of B. schlosseri (outlined in white better understood in the colonial ascidian B. schlosseri than dashed lines) surrounding a single colony of Botrylloides leachi,a species closely related to Botryllus (red dashed lines). in any other invertebrate system. Ascidians are soft-bodied invertebrate chordates (Phylum Chordata) that belong to the Subphylum Tunicata, a clade that diverged from its sister taxon, the Craniata (including the vertebrates), over cellulose matrix (the tunic), interconnected by a ramifying 600 Ma. The life cycles of botryllid ascidians such as and anastomosing blood vascular system (Figure 1(b)). B. schlosseri offer many opportunities for allorecognition Colony size has no intrinsic physiological or structural limit; consequently,
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