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The Society for Integrative and Comparative Biology
Self/non-self Discrimination in Basal Metazoa: Genetics of Allorecognition in the Hydroid Hydractinia1
1 Department of Biology, University of New Mexico, Albuquerque, New Mexico 87131
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Colonial basal metazoans often encounter members of their own species as they grow on hard substrata, with the encounters typically resulting in either fusion of close relatives or rejection between unrelated colonies. These allorecognition responses play a critical role in maintaining the genetic and physiological integrity of the colony. Allorecognition responses in basal metazoans are controlled by highly variable genetic systems. The molecular nature of such systems, however, remains to be determined. Current efforts to identify the genes and molecules controlling allorecognition in basal metazoans have followed two pathways: identification of molecules differentially expressed in incompatible interactions, and positional or map-based cloning of allorecognition genes. Most studies following the first approach have been performed with marine demosponges, while those following the second approach have centered on the cnidarian of the genus Hydractinia. Here, I discuss the latter, focusing primarily on the genetic control of allorecognition responses.
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Sessile colonial invertebrates have the ability to distinguish between their own tissues and those of unrelated members of the same species (Grosberg, 1988
). Typically, closely related colonies fuse, whereas unrelated conspecifics reject. These allorecognition responses have been recognized for more than a century (Bancroft, 1903) and have been unequivocally observed in the colonial basal metazoan phyla Porifera and Cnidaria (e.g., Teissier, 1929; Hauenschild, 1954, 1956; Müller, 1964; Theodor, 1970; Van de Vyver, 1970; Hildemann et al., 1977; Lubbock, 1980; Bigger et al., 1981; Hildemann and Linthicum, 1981). Allorecognition in colonial invertebrates plays a critical role in maintaining the physiological and genetic integrity of the colony. These organisms live permanently attached to hard surfaces, where cell-to-cell contact between conspecifics is of common occurrence. Fusion between allogeneic colonies might confer immediate advantage to the chimera by virtue of increasing its size. Indeed, in sessile colonial invertebrates size is positively correlated with fecundity and viability (Buss, 1990). Chimerism, however, is not risk free. Colonial invertebrates of different phyla have in common multipotent stem cells which are able to differentiate into germ and somatic cell lineages at any time during ontogeny (Buss, 1982, 1987). Cell lineages composing a chimera may vary widely in their gametic versus somatic investment (Buss, 1987). If one component of the chimera produces a disproportionately larger fraction of gametes than the other, then a parasitic relationship is established (Buss, 1987; Stoner and Weissman, 1996; Stoner et al., 1999). The parasitized partner's genetic representation declines in the next generation, and it heads towards an evolutionary dead end. It is conceivable, therefore, that colonial invertebrates are adapted to prevent somatic fusion between unrelated conspecifics as a mechanism to avoid germ cell parasitism. This adaptation involves highly discriminatory allorecognition systems and associated effector mechanisms.
Despite the biological significance of allorecognition and its widespread occurrence, the genes and molecules that control the response have not been identified in any invertebrate animal. Among basal metazoans, three model systems, two sponges and a cnidarian, have been widely employed in the search for allorecognition determinants. Most studies on sponge allorecognition have been performed with the marine demosponges Suberites domuncula and Geodia cydonium (Müller and Müller, 2003). Interactions between incompatible sponges activate exopinacocytes and various mesohyl cell types (Gaino et al., 1999). The involvement of these cells in the effector phase of allorecognition varies according to the species, and may involve cytotoxicity, phagocytosis, and synthesis of collagen barriers. Several molecules have been found to be differentially expressed in allogeneic interactions. These include circular proteoglycans known as spongicans (Fernandez-Busquets and Burger, 2003), allograft inflammatory factor-1 (Kruse et al., 1999), Tcf-like transcriptor factor (Müller et al., 2002), and other cytokine-like molecules (Müller and Müller, 2003). While these proteins play a role in the complex series of events triggered by allogeneic interactions, the recognition molecules that initiate such effector responses remain to be identified.
Cnidarians display a diverse set of effector responses against allogeneic tissues (Buss et al., 1984). These include extrusion of mesenterial filaments, differentiation of sweeper tentacles, induction of acrorhagi, and development of hyperplastic stolons. While allorecognition phenomena have been demonstrated in various cnidarian species, the genetic bases of the response have received extensive attention only in the hydractiniid hydroid Hydractinia echinata and its sister species Hydractinia symbiolongicarpus. In these species, segregation of allorecognition responses in crosses derived from field-collected colonies often defy simple Mendelian models (Hauenschild, 1954; Grosberg et al., 1996). Yet, when the genetic background is homogenized by inbreeding, fusibility segregates in a single chromosomal interval (Mokady and Buss, 1996). Here, I review the biology of allorecognition in H. symbiolongicarpus, and discuss recent studies that contribute to deciphering its genetic control.
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NATURAL HISTORY OF ALLORECOGNITION IN HYDRACTINIA SYMBIOLONGICARPUS |
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Hydractinia symbiolongicarpus (Cnidaria, Hydrozoa) is a colonial athecate hydroid found in near-shore waters of the northeastern United States. It grows as a surface incrustation on gastropod shells inhabited by the hermit crab Pagurus longicarpus (Buss and Yund, 1989
). Colonies are diploblastic and composed of three morphological structures: polyps, stolons and the stolonal mat (Fig. 1). Polyps are feeding structures and gamete carriers, and are embedded in the stolonal mat, a two-dimensional basal plate that consists of two ectodermal layers sandwiching a network of endodermal canals. These endodermal canals provide vascular continuity between the polyps' gastric cavities and may extend beyond the stolonal mat, in which case they are called stolons. Colonies release their gametes to the ocean where fertilization occurs. Fertilized eggs develop into crawling planula larvae which settle on hermit crab-occupied shells, and subsequently metamorphose into primary polyps. As stolons extend, bifurcate, and anastomose, new polyps bud from the stolons yielding thus a mature colony (Ballard, 1942; Berking, 1991).
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Allorecognition responses in Hydractinia are better understood than in perhaps any other colonial invertebrate (e.g., Teissier, 1929
; Schijfsma, 1939; Crowell, 1950; Hauenschild, 1954, 1956; Müller, 1964, 1967; Toth, 1967; Ivker, 1972; Gallien and Govaere, 1974; Buss et al., 1984; Buss et al., 1985; Lange et al., 1989; Feldgarden and Yund, 1992; Lange et al., 1992; Hart and Grosberg, 1999). Contact between Hydractinia colonies results in one of three outcomes: Fusion: After contact, compatible colonies dissolve their periderm coat and, within an hour, they adhere to one another by their epithelial cells. Two to four hours post-contact, colonies establish a common gastrovascular system forming a permanent chimera (Fig. 2A).
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Rejection: Upon contact, incompatible colonies fail to adhere, and within the first 12 hours, interacting tissues begin to swell due to massive migration of "stinging cells" or nematocytes, phylum-defining cells which contain specialized organelles called nematocysts. Nematocysts discharge a harpoon-like thread which delivers toxins causing extensive tissue destruction in the opponent (Müller, 1964
; Buss et al., 1984). Subsequent rejection takes two forms depending upon the colony morphology (Buss and Grosberg, 1990). Encounters between incompatible stoloniferous colonies (i.e., those with predominance of free stolons over stolonal mat) result in aggressive rejections (Fig. 2B) and are characterized by the induction of a specialized organ of defense, the hyperplastic stolon (Ivker, 1972). In these reactions, differentiation and recruitment of nematocytes continue until one colony has eliminated the other (Buss et al., 1984; Lange et al., 1989). Confrontations between stolonless colonies (i.e., those with predominance of stolonal mat over free stolons), produce passive rejections (Fig. 2C). These responses are characterized by the secretion of a fibrous matrix by both colonies, accompanied by cessation of growth along the contact margin (Buss and Grosberg, 1990).
Transitory fusion: In this reaction, colonies initially fuse only to separate days or weeks later (Hauenschild, 1954; Shenk and Buss, 1991; Grosberg et al., 1996; Gild et al., 2003; Cadavid et al., 2004). When initial fusion is established through the stolons, the reaction is characterized by initial occlusion of vascular spaces, followed by local necrosis and separation of interacting stolons (Shenk and Buss, 1991). When initial fusion is established through the stolonal mats, a necrotic band appears at the point where colonies initially contacted. This band subsequently spreads to form a line spanning the original contact zone. The emergence of the necrotic line is accompanied by occlusion of the once fused endodermal canals. Within days or weeks after the first appearance of the necrotic line, colonies separate from one another. From this point on, the response is indistinguishable from a passive rejection, except at the growing edges of the contact zone which, upon contact, display the same time course and phenomenology described above (Cadavid et al., 2004). Transitory fusion may in fact represent a composite of phenotypes that vary in time course, progression and developmental regulation. Transitory fusion might confer size-dependent benefits to the chimera, avoiding, at the same time, the risks of cell parasitism by rejecting prior the onset of sexual maturity (Buss and Shenk, 1990). This notion, however, has been challenged by Gild et al. (2003). These authors found a decrease of growth rates during the fusion stage of transitory fusion, followed by recovery to normal growth after separation. Furthermore, they offered evidence of free transit of gastrovascular fluid, perhaps including cells, among colonies during fusion stages of transitory interactions.
At least three lines of evidence suggest that allorecognition in Hydractinia is ontogenetically modulated. First, only post-metamorphic tissues display allorecognition responses; embryos and larvae fuse indiscriminately (Fuchs et al., 2002). Second, as recently reported by Wilson and Grosberg (2004), there is a progressive change in allorecognition thresholds at very early post-metamorphic stages. Specifically, fusion frequencies between pairs of full-sibs decreased from 73% 3 days after settlement to 58% in 12-day old colonies. The period of maximum decline occurred during the first 3–4 days post-metamorphosis, which might correspond to a period in which the effector mechanisms become fully competent. Third, Shenk and Buss (1991) observed a late ontogenetic shift in allorecognition specificity in H. symbiolongicarpus. This shift occurred at the onset of sexual maturity and was characterized by a decrease in fusion frequencies between parents and offspring and by the expression of transitory fusion.
Allorecognition responses in laboratory settings can be scored by two types of fusibility tests, the standard colony assay and the polyp assay. In standard colony assays (Buss et al., 1984), a fragment of stolonal mat containing 3–5 polyps from each of the colonies to be tested are placed 0.5 cm from one another on a glass slide and kept in position by a string. Tissues attach to the glass within 24–48 hr and the string is then removed. Colonies grow into contact to one another within 3–6 days and are periodically evaluated for fusibility.
In the polyp fusibility test (Lange et al., 1992), polyps from the two contesting colonies are excised and held with their cut ends appressed. Compatible polyps develop continuous endodermal and ectodermal cell layers and a common gastric cavity within 12–24 hr. Incompatible polyps, on the other hand, separate. An important distinction between the two fusibility assays is that transitory fusion is only detected in standard colony tests, i.e., interactions that display transitory fusion in the colony assay behave as permanent fusions in polyp assays (Cadavid et al., 2004) It remains to be formally investigated whether alternative tissue-specific mechanisms control allorecognition in Hydractinia.
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GENETICS OF ALLORECOGNITION IN HYDRACTINIA |
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The transmission genetics of allorecognition in Hydractinia was first addressed in the mid-1950s and has been a focus of debate since then. Based on a series of breeding experiments, Hauenschild (1954
, 1956) proposed that allorecognition could be formally explained by assuming a single locus bearing co-dominantly expressed alleles where fusion results from matching one or two alleles. However, some of his results, particularly unexpected phenotypes in the F1, F2, and offspring of F1 x F2, deviated from single-locus expectations (Hauenschild, 1954). Although transitory fusion was observed in his crosses, the response was interpreted initially as fusion (Hauenschild, 1954) and later as rejection (Hauenschild, 1956). Hauenschild's genetic model, therefore, did not account for transitory fusion. Du Pasquier (1974) reinterpreted Hauenschild's data, and noted that some of the deviations from the single-locus expectations could be explained under a gene-dose effect model where "one haplotype difference results in a weaker [rejection] reaction than two haplotype differences," where this weaker reaction may be interpreted as transitory fusion. Here, haplotype is used in the context of a combination of loci present in a defined area of the genome. Furthermore, he suggested that the allorecognition locus proposed by Hauenschild might be composed of subloci that recombine to generate new allotypic specificities.
Deviations from simple Mendelian patterns were also reported by Grosberg et al. (1996). Based on breeding experiments and simulation analyses, they proposed that allorecognition responses in Hydractinia result from a dosage-dependant interaction between a hypothesized set of 5 unlinked loci with 5–7 alleles per locus. Mokady and Buss (1996), starting from the hypothesis that allorecognition is controlled by a main polymorphic locus modified by secondary loci, inbred H. symbiolongicarpus to standardize the effects of those secondary loci on the expression of allorecognition. Applying a conventional incross/intercross/ backcross breeding strategy, they observed that allorecognition segregated in a single chromosomal interval as a one-locus trait with co-dominantly expressed alleles, such that colonies fuse if they share one or two alleles. However, Mokady and Buss did not observed transitory fusion segregating in their lines and hence this response was not incorporated into their model.
More than five decades after Hauenschild's pioneering experiments, a robust model explaining the transmission genetics of allorecognition in Hydractinia is yet to be postulated. Available information suggests that the phenomenon is a complex trait (Grosberg et al., 1997). The complicated inheritance of complex traits is often attributed to the fact that such traits are affected by the simultaneous variation of many genes that interact in complex ways. These genes are referred to as the genetic background, and variation in the genetic background often has a major effect on the expression of a given gene. In addition, various epigenetic factors may affect the expression of a complex trait. At the core of the genetics of complex traits lies a non-linear relationship between genetic variation and trait variation. The inbreeding program initiated by Mokady and Buss allowed the identification of an individual allorecognition locus by standardizing the effects of the genetic background on the expression of the trait. A complete genetic characterization of allorecognition in Hydractinia will require a systematic replication of Mokady and Buss' approach using several genetic lines. Further development of such inbreeding program is considered in detail in the next sections.
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GENETIC CHARACTERIZATION OF A GENE COMPLEX CONTROLLING ALLORECOGNITION IN HYDRACTINIA |
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The inbreeding program of Mokady and Buss (1996)
is depicted in the shaded zone of Figure 3. From this starting point, Cadavid et al. (2004) developed two inbred lines (lines 33 and 41, Fig. 3) and a third line genetically identical to line 33 except at a single chromosomal interval (i.e., a congenic line). Inbred lines were generated by brother-sister matings of fusible offspring for several generations. Colonies from an inbred line fused to one another and rejected those of the other line. Hence, these lines were fixed for a single allotypic specificity and were hypothesized to be homozygous for different alleles at an allorecognition (alr) locus (i.e., the hypothesized genotype of the 33 line is alr-f/-f and that of the 41 line is alr-r/-r). The congenic line was generated by repeated backcrossing of the 41 line into the 33 line. Congenic animals are identical to the 33 line colonies at nearly all loci excepting those tightly linked to the alr locus. Two genotypes, alr-f/-f and alr-f/-r, segregate in the congenic line (Cadavid, 2001). As discussed in the previous section, this line is a valuable tool for genetic and molecular analysis as variation in fusibility is largely limited to the chromosomal region introgressed by the backcrossing process.
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To study the transmission genetics of allorecognition in these Hydractinia lines, Cadavid (2001)
crossed two congenic animals which fused both inbred lines (hypothesized genotypes, alr-f/-r x alr-f/-r), and generated 81 offspring (named 431 population). Under a single-locus model for allorecognition, this population is expected to segregate into three genotypic classes, alr-f/-f, alr-f/-r, alr-r/-r, with ratios of 1:2:1, respectively. Thus, if the population is tested against one of the inbred lines, fusion and rejection are expected to segregate in a 3:1 ratio. Indeed, a ratio not significantly different from 3:1 was observed in this congeneic population (Table 1). However, two of the 81 colonies displayed transitory fusion against one inbred line (Cadavid et al., 2004). Clearly, the single-locus model for allorecognition does not explain the expression of transitory fusion at low frequency with permanent fusion and rejection segregating as a single Mendelian trait.
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The fact that Mokady and Buss (1996)
did not observe transitory fusion in their analysis appears paradoxical since the H. symbiolongicarpus lines used by Cadavid et al. (2004) were derived from their breeding program. This discrepancy is most likely explained by the way fusibility tests were performed. Mokady and Buss scored their colonies exclusively by the polyp fusion test, and, as mentioned before, transitory fusion is only detected in standard colony tests. Thus, it is likely that transitory fusion cases remained cryptic in the lines until the congenic population was characterized by colony assays.
The simplest genetic model accounting for an inheritance pattern of allorecognition where transitory fusion is expressed at low frequencies with permanent fusion and rejection otherwise segregating as a single Mendelian trait is that of dose-dependent interaction between two linked loci (Cadavid et al., 2004). Specifically, colonies fuse if they share one or two haplotypes, they reject if they share no haplotypes, and display transitory fusion if they share only one allele at one haplotype and no alleles at the other. Under this two-locus model the inbred lines are considered homozygous at both allorecognition loci, alr1 and alr2, where alr1 has alleles f and r, and alr2 has alleles 
and ß. Thus, the 33 line is hypothesized to be alr1-f, alr2-/ar1-f, alr2-, hereafter f/f, and the 41 line is hypothesized to be alr1-r, alr2-ß/alr1-r, alr2-ß, hereafter rß/rß. Likewise, a colony fusing both inbred lines is hypothesized to be double-heterozygote with genotype alr1-f, alr2-/alr1-r, alr2-ß, hereafter f/rß. Finally, colonies displaying transitory fusion against the line 33 and fusing with the line 41 have the recombinant genotype r/rß (or rß/fß), whereas colonies displaying transitory fusion against the line 41 and fusing with line 33 possess the recombinant genotype f/fß (or f/r). The predictions of this two-locus model in the context of the H. symbiolongicarpus lines are presented in Table 2.
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Three crosses were made to test the two-locus model (Cadavid et al., 2004
). One cross involved two colonies that do not display transitory fusion against the inbred lines (hypothesized genotypes f/rß x f/f). For the other two crosses, colonies displaying transitory fusion were mated with colonies not displaying transitory fusion (hypothesized genotypes f/fß x f/ f and rß/rß x r/rß) (Fig. 4). The offspring of these three populations were tested for fusibility against both inbred lines by colony assays. In the population derived from parents that do not display transitory fusion, fusion and rejection segregation did not differed significantly from the expected 1:1 ratio. Transitory fusion appeared in 2.2% of the offspring (11 out of 490 siblings). In the two crosses involving a parent displaying transitory fusion, a ratio not significantly different from 1:1 for rejection and transitory fusion was observed (Fig. 4). Segregation of fusibility in these crosses, therefore, is consistent with an hypothesized allorecognition complex, ARC, comprised of at least two linked loci bearing co-dominantly expressed alleles, such that colonies fuse if they share at least one haplotype, reject if they share no haplotypes, and display transitory fusion if they share only one allele in one haplotype and none in the other. Thus, standardization of the genomic background through inbreeding has allowed identifying a chromosomal region containing at least two linked loci. Genetic characterization of additional loci involved in allorecognition would require a similar strategy on different inbred lines.
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Traits that segregate in single chromosomal intervals can be localized in a defined chromosomal region, even in organisms with otherwise uncharacterized genomes (Tanksley et al., 1995
). Using defined crosses, pools of DNA are generated from homozygous offspring differing in the phenotype of interest. Molecular markers linked to the target region are identified by presence in one pool and absence in the other (Michelmore et al., 1991). A preferred method for high-throughput generation of molecular markers is amplified fragment length polymorphism (AFLP) (Vos et al., 1995). With sufficient effort, AFLP markers can be identified at close proximity of the gene(s) of interest.
Following that approach, Cadavid et al. (2004) found four AFLP markers polymorphic between pools of congenic animals differing in their allotypic specificities. A large backcross population (n = 490, f/f x f/rß) was used to map the ARC-containing chromosomal interval. In this population, the only segregating parental haplotype is rß. All four markers (R18, R28, 174, 194) segregated as expected for a dominant Mendelian locus with no significant deviation from a 1:1 ratio of presence to absence (Cadavid et al., 2004). Multi-point analysis with these four markers and the two allorecognition loci characterized genetically in the lines, alr1 and alr2, produced a map where ARC is delineated at 3.4 cM such that alr1 is flanked by markers 194 and 18 at 0.9 and 1.9 cM, respectively, and alr2 is flanked by marker R28 at 0.2 cM (Fig. 5). A total of 13 animals showed recombination in the ARC region. Eleven of these recombinant animals had a crossing-over between alr1 and alr2, and as predicted by the two-locus model, they were precisely the ones that displayed transitory fusion against rß/rß animals (see Fig. 4).
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Since its discovery at the onset of the 20th century, allorecognition in colonial invertebrates has attracted the attention of ecologists, geneticists, evolutionary biologists, and comparative immunologists. At the center of such widespread interest lies the question of what are the bases for the exquisite discriminatory ability of allorecognition systems. Invertebrate allorecognition systems discriminate between self and non-self with high precision, suggesting that those systems are endowed with extremely high levels of genetic variation. This variation may in theory be attained through a variety of genetic systems, ranging from a single, highly polymorphic locus to a set of loci with relatively low levels of polymorphism. An example of the former is found in ascidians of the genus Botryllus, where a single locus with multiple co-dominant alleles controls allorecognition responses. Botryllus colonies sharing at least one allele at this locus fuse, whereas those not sharing alleles reject (Oka and Watanabe, 1957
; Scofield et al., 1982). Segregation of allorecognition responses in natural populations of Hydractinia often violates the expectations of the Botryllus model, suggesting a more complex genetic system.
To decipher the genetics of allorecognition in Hydractinia, Mokady and Buss (1996) and Cadavid et al. (2004) generated defined genetic lines with the goal of homogenizing variation in most of the genome, excepting a chromosomal region controlling allorecognition. In these lines, classical genetics analyses suggested the existence of at least two loci (alr1 and alr2) segregating in a single chromosomal interval. Molecular markers generated by pooled segregant analyses circumscribed a 3.4 cM region containing the two loci identified by classical methods. Colonies displaying transitory fusion had a recombination between alr1 and alr2. Allorecognition outcomes in these lines can be predicted by a simple rule of dose-dependent interaction of two linked loci. Thus, colonies fuse if they share at least one haplotype, reject if they share no haplotypes, and display transitory fusion if they share only one allele in one haplotype and none in the other.
The fact that hydroid allorecognition is controlled by at least one gene complex may have an adaptive explanation. Hydractinia larvae recruit and metamorphose on shells occupied by the hermit crab in a site-specific fashion, such that allogeneic encounters are likely to occur. Fusion entails the risk of establishing cell-lineage parasitism, but this risk can be partially ameliorated by restricting fusion to close relatives. An allorecognition system having one polymorphic locus (as in the ascidian Botryllus) would serve as a kin recognition system, but its effectiveness is expected to be a function of the number and frequency of the alleles in the population. Common alleles would promote fusion between unrelated individuals and, consequently, the establishment of germ cell parasitism. A second allorecognition locus linked to the first one would largely eliminate the frequency-dependent effect as the probability of fusion between unrelated individuals would be a function of the allele frequency multiplied by the recombination fraction between the two loci.
Identification of the allorecognition determinants and the genes encoding them has proven difficult. Previous attempts to identify them have focused on the search for plausible candidate genes by either structural similarities to their putative vertebrate counterparts, or by analogy to other recognition systems. Both efforts have proven fruitless, and in retrospect, the problem seems to demand a strategy that makes no a priori assumptions as to the identity of the gene product, i.e., positional cloning. A map is an essential first step in positional cloning the ARC loci. Comparable efforts are underway using the ascidian Botryllus schlosseri where the Fu/HC locus has been mapped at a fraction of cM (De Tomaso et al., 1998; De Tomaso and Weissman, 2003). With the availability of maps spanning relevant intervals in both Botryllus and Hydractinia, the tools are in hand to at last isolate the colonial invertebrate allorecognition determinants.
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ACKNOWLEDGMENTS |
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I thank Rick Grosberg, Alan Kohn and an anonymous reviewer for comments on the manuscript. Support provided by the National Science Foundation (IBN 0315968).
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FOOTNOTES |
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1 From the Symposium Model Systems for the Basal Metazoans: Cnidarians, Ctenophores, and Placozoans presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 5– 9 January 2004, at New Orleans, Louisiana.
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