The genetic control and consequences of kin recognition by the larvae of a colonial marine invertebrate

Grosberg, Richard K.; Quinn, James

doi:10.1038/322456a0

Cited by 269 publications

(216 citation statements)

References 30 publications

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“…Buss (1982) suggested that the increased size of chimeras over clones would benefit chimeras when sizespecific ecological processes, such as competitive ability, predation risk and fecundity, existed. In support of this, larger size increases growth rate and survival in B. schlosseri and in corals that are known to form chimeras with close kin (Hughes & Jackson 1980;Jokiel & Morrissey 1986;Grosberg & Quinn 1986). In addition, a recent study has shown that grouping by sperm in wood mice increases swimming velocity (Moore et al 2002).…”

Section: Discussionmentioning

confidence: 97%

The costs and benefits of being a chimera

Foster

Fortunato

Strassmann

et al. 2002

Proc. R. Soc. Lond. B

121

128

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Most multicellular organisms are uniclonal. This is hypothesized to be because uniclonal organisms function better than chimeras (non-clonal organisms), owing to reduced levels of internal genetic conflict. We tested this idea using the social amoeba or slime mold Dictyostelium discoideum. When starving, the normally solitary amoebae aggregate to form a differentiated multicellular slug that migrates towards light and forms a fruiting body, facilitating the dispersal of spores. We added 10 7 amoebae to Petri plates containing 1, 2, 5 or 10 clones mixed together. We found an intrinsic cost to chimerism: chimeric slugs moved significantly less far than uniclonal slugs of the same size. However, in nature, joining with other clones to form a chimera should increase slug size, and larger slugs travel further. We incorporated this size effect into a second experiment by giving chimeras more cells than single clones (single clones had 10 6 cells, two-clone chimeras had 2 × 10 6 cells and so on). The uniclonal treatments then simulated a clone in a mixture that refuses to form chimeras. In this experiment, chimeras moved significantly further than the uniclonal slugs, in spite of the intrinsic cost. Thus, chimerism is costly, which may be why it evolves so seldom, but in D. discoideum the benefits of large size appear to compensate.

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Section: Discussionmentioning

confidence: 97%

The costs and benefits of being a chimera

Foster

Fortunato

Strassmann

et al. 2002

Proc. R. Soc. Lond. B

121

128

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“…Indeed, self-matching may be favoured in nepotistic situations, in which animals need to identify individuals to whom they are most closely related (e.g. Getz & Smith 1986;Grosberg & Quinn 1986;Manning et al 1992;Petrie et al 1999). In contrast, additional referents (such as parents and siblings) should be used in mate-choice decisions, to help animals identify all individuals to whom they are closely related (e.g.…”

Section: Introductionmentioning

confidence: 99%

Kin recognition and the ‘armpit effect’: evidence of self–referent phenotype matching

Mateo

Johnston

2000

Proc. R. Soc. Lond. B

188

125

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In species with multiple paternity or maternity, animals may best assess their relatedness to unfamiliar conspeci¢cs by comparing their own phenotype(s) with those of unidenti¢ed individuals. Yet whether animals can recognize kin through self-matching is controversial. Because golden hamsters (Mesocricetus auratus) mate multiply and can produce multiply sired litters, they were tested for their ability to use selfmatching for kin recognition. Hamsters that were reared only with non-kin since birth responded di¡erentially to odours of unfamiliar relatives and non-relatives. Postnatal association with kin was not necessary for this discrimination. Prenatal learning was unlikely because of delayed production and perception of social odours. To our knowledge, this is the ¢rst demonstration that a vertebrate can use its own phenotype for kin-recognition purposes without prior experience with kin. By using itself as a referent, rather than its siblings or parents, a golden hamster may be better able to direct nepotism towards the most appropriate individuals. Kin discrimination via self-inspection may be especially important in nepotistic contexts (to identify most closely related conspeci¢cs), whereas inclusion of the phenotypes of close kin as referents may be favoured in mate-choice contexts (to identify all related individuals).

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“…To the extent that this specificity is genetically controlled, the loci governing invertebrate allorecognition specificity may exhibit polymorphism that rivals, or exceeds, levels recorded at loci in the vertebrate Major Histocompatibility Complex (Potts and Wakeland 1990;Hughes and Nei 1992;Brown and Ecklund 1994;Hedrick 1994), as well as loci associated with gametophytic incompatibility systems in angiosperms (Ebert et al 1989). High levels of allotypic specificity could, however, result from any number of genetic alternatives, ranging from one or a few loci with tens to hundreds of alleles per locus (characteristic of populations of botryllid ascidians : Milkman 1967;Mukai and Watanabe 1975a,b;Scofield et al 1982;Grosberg and Quinn 1986;Rinkevich and Saito 1992;Yund and Feldgarden 1992;Rinkevich et al 1994) to numerous independent loci with relatively low levels of allelic variation (Curtis et al 1982). The ability to distinguish among these genetic alternatives, and to circumscribe the rules governing compatibility, determines how the expression of allorecognition-dependent behaviors influences the evolution of allotypic variation.…”

Section: Simulated Frequencies Of Compatibility In Full and Halfmentioning

confidence: 99%

“…No studies comprehensively quantify these costs and benefits. Moreover, because the genetic polymorphism that characterizes most invertebrate allorecognition systems should restrict fusion to close relatives and aggression to more distantly related individuals, the costs and benefits of both types of behavior must be adjusted according to kinship of the interactants (Buss and Green 1985;Grosberg and Quinn 1986;Reeve 1989;Grafen 1990), an unknown quantity in most instances.…”

Section: 0 -R ---------------mentioning

confidence: 99%

EVOLUTIONARY GENETICS OF ALLORECOGNITION IN THE COLONIAL HYDROID HYDRACTINIA SYMBIOLONGICARPUS

1996

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Abstract.-Many sedentary, clonal marine invertebrates compete intensively with con specifics for habitable space. Allorecognition systems mediate the nature and outcome of these intraspecific competitive interactions, such that the initiation of agonistic behavior and the potential for intergenotypic fusion depend strongly on the relatedness of the contestants. The dependence of these behaviors on relatedness, along with the extraordinary precision with which self can be discriminated from nonself, suggest that allorecognition systems are highly polymorphic genetically. However, allotypic specificity of this sort could be produced by any number of genetic scenarios, ranging from relatively few loci with abundant allelic variation to numerous loci with relatively few alleles per locus. At this point, virtually nothing is known of the formal genetics of allorecognition in marine invertebrates; consequently, the evolutionary dynamics of such systems remain poorly understood. In this paper, we characterize the formal genetics of allorecognition in the marine hydrozoan Hydractinia symbiolongicarpus. Hydractinia symbiolongicarpus colonizes gastropod shells occupied by hermit crabs. When two or more individuals grow into contact, one of three outcomes ensues: fusion (compatibility), transitory fusion (a temporary state of compatibility), and rejection (incompatibility, often accompanied by the production of agonistic structures termed hyperplastic stolons). Observed patterns of compatibility between unrelated, half-sib pairs, and full-sib pairs show that unrelated and half-sib pairs under laboratory culture have a very low probability of being fusible, whereas full sibs have a roughly 30% rate of fusion in experimental pairings. The genetic simulations indicate that roughly five loci, with 5-7 alleles per locus, confer specificity in this species. In ecological terms, the reproductive ecology of H. symbiolongicarpus should promote the cosettlement of kin, some of which should be full sibs, and some half sibs. Thus, there is potential for kin selection to playa major role in the evolution of the H. symbiolongicarpus allorecognition system. In genetic terms, this system conforms to theoretical predictions for a recognition system selected to distinguish among classes of kin, in addition to self from nons elf.

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The genetic control and consequences of kin recognition by the larvae of a colonial marine invertebrate

Cited by 269 publications

References 30 publications

The costs and benefits of being a chimera

The costs and benefits of being a chimera

Kin recognition and the ‘armpit effect’: evidence of self–referent phenotype matching

EVOLUTIONARY GENETICS OF ALLORECOGNITION IN THE COLONIAL HYDROID HYDRACTINIA SYMBIOLONGICARPUS

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