Polymorphism in the Immunoglobulin-like Domains of the Receptor Tyrosine Kinase from the Sponge Geodia Cydonium

Sponges [Porifera] are the phylogenetically oldest phylum of the Metazoa. They are provided with both cellular and humoral allorecognition systems. The underlying molecules are not yet known. To study allorecognition in sponges we first determined the frequency of graft rejection in a natural population of the marine sponge Geodia cvdonium. We then determined, for the first time at the molecular level, the degree of sequence polymorphism in segments of one molecule which may be related to sponge allorecognition and host defense: the Ig-like domains from the receptor tyrosine kinase [RTK]. Thirty six pairs of auto- and allografts were assayed, either by parabiotic attachment or insertion of grafts. All of the autografts fused, while only two allografts fused and 34 pairs were incompatibile. Rejection among the parabiotic allografts was characterized by the formation of a collagenous barrier, while the allografts that were inserted into the host underwent destruction. At the molecular level we first cloned to completion the 5′-end of sponge RTK, which displays a Pro-Ser-Thr-rich sequence; this is thought to act as a module of cell adhesion proteins. Then we analyzed RT-PCR products of amplification across the two Ig-like domains of RTK (about 500 bp), from two pairs of fusing sponges and one pair of rejecting sponges. High levels of polymorphism were recorded, including 18 nucleotide-substitution positions and a tri-nucleotide deletion, which translate into 13 polymorphic amino acid positions. Two of the six sponges were scored as heterozygotes. Among 9 informative polymorphic sites that were tested for linkage disequilibrium, 11 pairwise comparisons were found to be significant, implying the possibility of distinguishable alleles in this locus. To the best of our knowledge this is the first report of polymorphism in Ig-like domains of a receptor from invertebrates that may be associated with allorecognition. This data attests also that fusion in sponges is not confined to genetically identical individuals.     

The importance of life-history stage and individual variation in the allorecognition system of a marine sponge

In marine invertebrates with complex life cycles, it may often be the case that trade-offs and behaviors differ between adult and larval stages. In this study, I examined the effects of life-history stage on allorecognition system function in the sponge, Haliclona sp. For sedentary marine invertebrates, allorecognition systems allow individuals to distinguish between genetically similar and distinct tissue they may encounter and are thought to reduce costly tissue fusion with individuals other than self or kin. Although it was found that sessile adults fused preferentially with self-tissue and exhibited a functioning allorecognition system, free-swimming larvae fused equally with sibling and non-sibling larvae resulting in swimming chimeras capable of successful metamorphosis, suggesting a stage-activated allorecognition system. In addition, adult sponges differed significantly in the propensity of their larvae to fuse suggesting variation in parental strategies. Analysis of larval swimming behavior indicated that larvae aggregate and are capable of increasing their encounters with other larvae and perhaps their probability of fusing in nature. The pursuit of fusion at this motile stage, along with evidence of a functioning adult allorecognition system, suggests that larvae may not express a recognition system, or that factors other than relatedness such as benefits to larval or adult chimeras, are involved in larval fusion and a stage-activated allorecognition system. In addition, this study demonstrates the presence of variation among individuals in the allorecognition system's ontogeny in the sponge Haliclona sp.     

EVOLUTIONARY GENETICS OF ALLORECOGNITION IN THE COLONIAL HYDROID HYDRACTINIA SYMBIOLONGICARPUS

Many sedentary, clonal marine invertebrates compete intensively with conspecifics 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 play a 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 nonself.     

Polymorphism in the Immunoglobulin-like Domains of the Receptor Tyrosine Kinase from the Sponge Geodia Cydonium

Sponges [Porifera] are the phylogenetically oldest phylum of the Metazoa. They are provided with both cellular and humoral allorecognition systems. The underlying molecules are not yet known. To study allorecognition in sponges we first determined the frequency of graft rejection in a natural population of the marine sponge Geodia cvdonium. We then determined, for the first time at the molecular level, the degree of sequence polymorphism in segments of one molecule which may be related to sponge allorecognition and host defense: the Ig-like domains from the receptor tyrosine kinase [RTK]. Thirty six pairs of auto- and allografts were assayed, either by parabiotic attachment or insertion of grafts. All of the autografts fused, while only two allografts fused and 34 pairs were incompatibile. Rejection among the parabiotic allografts was characterized by the formation of a collagenous barrier, while the allografts that were inserted into the host underwent destruction. At the molecular level we first cloned to completion the 5'-end of sponge RTK, which displays a Pro-Ser-Thr-rich sequence; this is thought to act as a module of cell adhesion proteins. Then we analyzed RT-PCR products of amplification across the two Ig-like domains of RTK (about 500 bp), from two pairs of fusing sponges and one pair of rejecting sponges. High levels of polymorphism were recorded, including 18 nucleotide-substitution positions and a tri-nucleotide deletion, which translate into 13 polymorphic amino acid positions. Two of the six sponges were scored as heterozygotes. Among 9 informative polymorphic sites that were tested for linkage disequilibrium, 11 pairwise comparisons were found to be significant, implying the possibility of distinguishable alleles in this locus. To the best of our knowledge this is the first report of polymorphism in Ig-like domains of a receptor from invertebrates that may be associated with allorecognition. This data attests also that fusion in sponges is not confined to genetically identical individuals.     

EVOLUTION OF ALLORECOGNITION IN BOTRYLLID ASCIDIANS INFERRED FROM A MOLECULAR PHYLOGENY

Despite the functional and phyletic ubiquity of highly polymorphic genetic recognition systems, the evolution and maintenance of these remarkable loci remain an empirical and theoretical puzzle. Many clonal invertebrates use polymorphic genetic recognition systems to discriminate kin from unrelated individuals during behavioral interactions that mediate competition for space. Space competition may have been a selective force promoting the evolution of highly polymorphic recognition systems, or preexisting polymorphic loci may have been coopted for the purpose of mediating space competition. Ascidian species in the family Botryllidae have an allorecognition system in which fusion or rejection between neighboring colonies is controlled by allele-sharing at a single, highly polymorphic locus. The behavioral sequence involved in allorecognition varies in a species-specific fashion with some species requiring extensive intercolony tissue integration prior to the allorecognition response, while other species contact opposing colonies at only a few points on the outer surface before resolving space conflicts. Due to an apparent species-specific continuum of behavioral variation in the degree of intercolony tissue integration required for allorecognition, this system lends itself to a phylogenetic analysis of the evolution of an allorecognition system. We constructed a molecular phylogeny of the botryllids based on 18S rDNA sequence and mapped allorecognition behavioral variation onto the phylogeny. Our phylogeny shows the basal allorecognition condition for the group is the most internal form of the recognition reaction. More derived species show progressively more external allorecognition responses, and in some cases loss of some features of internal function. We suggest that external allorecognition appears to be a secondary function of a polymorphic discriminatory system that was already in place due to other selective pressures such as gamete, pathogen, or developmental cell lineage recognition.     

KIN INTERACTIONS IN A COLONIAL HYDROZOAN (HYDRACTINIA SYMBIOLONGICARPUS): POPULATION STRUCTURE ON A MOBILE LANDSCAPE

Many sessile colonial organisms intensively compete with conspecifics for growing space. This competition can result in either cooperative fusion or aggressive rejection between colonies, and some species have evolved highly polymorphic genetic systems that mediate the outcome of these interactions. Here we demonstrate the potential for interactions among close kin as the basis for the evolutionary maintenance of a genetically polymorphic allorecognition system in the colonial hydroid Hydractinia symbiolongicarpus, which lives on gastropod shells occupied by hermit crabs. Fusion between hydroids in the laboratory is restricted mainly to encounters between full siblings, whereas other encounters result in aggressive rejection. Natural selection acting on the costs or benefits of fusion between colonies could be responsible for the present maintenance of such a highly specific behavioral response, but only if encounters between fusible colonies still occur in contemporary populations. The large size of these hydroid populations and the mobility of the crabs should limit the potential for interactions among closely related hydroids on the same shell. However, RAPD polymorphisms among a large sample of hydroids from a population off the coast of Massachusetts indicate that genetically similar colonies are often found together on the same shell. Some genetic distances between colonies on the same shell were low relative to genetic distances between colonies on different shells or genetic distances between known full siblings from laboratory matings. We conservatively estimate that 2–18% of co-occurring colonies may be full sibling pairs. These observations suggest that encounters between genetically similar hydroids are common, despite the mobile nature of their habitat, and these encounters may provide frequent opportunities for natural selection to influence the evolution of cooperative and agonistic behaviors and their polymorphic genetic basis.     

Freshwater sponge (Porifera: Spongillidae) distribution across a landscape: Environmental tolerances,habitats, and morphological variation

Freshwater sponges are important to ecosystem functioning; however, information about their biogeography and interspecific variation is fragmentary, limiting our ability to assess their role. Although the specific epithets of two common species suggest that sponges found in lentic habitats are Spongilla lacustris, and those found in lotic habitats are Ephydatia fluviatilis, the number of sponge species in the UK is unresolved. We sampled sponges in a variety of habitats and used both morphological and molecular (D3 domain of 28S rDNA) methods to identify six species, including the first record of Trochospongilla horrida. We contrasted species in terms of their environmental tolerances, habitats, and variation, and we expanded on the limited information available about the geographic distributions of these sponges. In our study, most sponge species colonized a variety of substrates, but exhibited different distributions. The most widespread sponge, S. lacustris, was present at lower mean water temperatures and was more often located above a latitude of 55°N. Ephydatia fluviatilis was the most common species in rivers, but was also located in lentic habitats. Salinity in anthropogenic habitats was not a significant factor for the presence of E. fluviatilis or the more patchily distributed species Eunapius fragilis. Instead, these species occurred more frequently at sites with negative oxidation–reduction potential. Sponge biodiversity may be affected by substrate availability in anthropogenic habitats, invasive species, and improved ability to recognize sponge taxa. Crucially, we provide foundation data as a prerequisite for future ecological evaluation.     

Model systems of invertebrate allorecognition

Nearly all colonial marine invertebrates are capable of allorecognition--the ability to distinguish between self and genetically distinct members of the same species. When two or more colonies grow into contact, they either reject each other and compete for the contested space or fuse and form a single, chimeric colony. The specificity of this response is conferred by genetic systems that restrict fusion to self and close kin. Two selective pressures, intraspecific spatial competition between whole colonies and competition between stem cells for access to the germline in fused chimeras, are thought to drive the evolution of extensive polymorphism at invertebrate allorecognition loci. After decades of study, genes controlling allorecognition have been identified in two model systems, the protochordate Botryllus schlosseri and the cnidarian Hydractinia symbiolongicarpus. In both species, allorecognition specificity is determined by highly polymorphic cell-surface molecules, encoded by the fuhc and fester genes in Botryllus, and by the alr1 and alr2 genes in Hydractinia. Here we review allorecognition phenomena in both systems, summarizing recent molecular advances, comparing and contrasting the life history traits that shape the evolution of these distinct allorecognition systems, and highlighting questions that remain open in the field.     

Self/nonself recognition in Cnidaria: contact to allogeneic tissue does not result in elimination of nonself cells in Hydra vulgaris

Although Cnidaria have no specialised immune cells, some colonial forms possess a genetic system to discriminate between self and nonself. Allorecognition is thought to protect them from fusion with genetically different individuals and to prevent germ line parasitism. Surprisingly, when grafting tissue of two species of the solitary freshwater polyp Hydra, we found within the contact zone phagocytozing epithelial cells which selectively eliminated cells from the other species (Bosch and David, 1986). This led us to speculate that Hydra, which never undergoes "natural transplantation", can differentiate between self and nonself (Bosch and David, 1986). In a previous paper (Kuznetsov et al., 2002) we described that cells which accumulate in the contact region of these interspecies grafts are apoptotic and that apoptosis is induced by impaired cell matrix contact. Thus, observations in such interspecies grafts did not give hints concerning the presence of a discriminative allorecognition system. To clarify whether this fundamental aspect of immunity is present in these phylogenetically old animals, we examined epithelial interactions between different strains of Hydra vulgaris. Here, we show that contact to allogeneic tissue does not evoke any response in terms of phagocytosis and elimination of allogeneic cells. We, therefore, question Hydra's ability to discriminate between self and nonself and propose that, in contrast to colonial cnidarians, the solitary polyp Hydra has either lost or substantially reduced this ability.     

DEVELOPMENTAL PLASTICITY,GENETIC VARIATION,AND THE EVOLUTION OF ANDROMONOECY IN SOLANUM HIRTUM (SOLANACEAE)

Studies of andromonoecious species have shown that sex expression (proportions of hermaphrodite and staminate flowers) is quite variable. It is not known, however, whether this variation is due to variation among individuals for genetically fixed patterns of allocation to staminate and hermaphrodite flowers (population level variation) and/or to developmental plasticity of individuals in a heterogeneous environment (organismal level variation). Distinguishing between these two levels of variation is important for understanding the evolution of andromonoecy. This study investigates levels of variation in sex expression in the andromonoecious Solanum hirlum. Sex expression in this species is shown to be plastic among individuals of the same genotype (organismal level variation) and determined, in part, by the resource status of the individual. Among the genotypes examined there is also genetic variation for developmental plasticity. Thus, developmental plasticity can potentially respond to selection, and the evolution of this developmental system may have been instrumental in the establishment and maintenance of andromonoecy in S. hirtum.     

Integrative taxonomy of calcareous sponges (subclass Calcinea) from the Peruvian coast: morphology,molecules, and biogeography

Understanding of evolution and systematics of Calcarea (Porifera) have not yet met a corresponding increase in the knowledge of diversity and distribution of these sponges in several parts of the world. Peru is an emblematic example of this lack of taxonomic knowledge, as only three shallow‐water species of sponges have hitherto been reported from its 3000 km coast. With the aim of studying sponges of Peru, an integrative taxonomy approach (morphology, molecules, and biogeography) was used in order to achieve sound species identifications. The first findings of Peruvian calcareous sponges are presented here. Eight species are described in the subclass Calcinea, of which five are new to science. The retrieved biogeographical patterns are either locally endemic, widespread, or discontinuous over large areas. Clathrina antofagastensis was previously known from Chile, while C. aurea and Ernstia tetractina had been reported from the Atlantic (Brazil), and thus represent the first genetically confirmed tropical amphi‐American distributions of species not yet found on both sides of the Isthmus of Panama. Our results reveal a richer Tropical East Pacific sponge fauna than the Warm Temperate South‐Eastern Pacific one. © 2015 The Linnean Society of London     

Phenotypic and genetic diversity in aposematic Malagasy poison frogs (genus Mantella)

Intraspecific color variation has long fascinated evolutionary biologists. In species with bright warning coloration, phenotypic diversity is particularly compelling because many factors, including natural and sexual selection, contribute to intraspecific variation. To better understand the causes of dramatic phenotypic variation in Malagasy poison frogs, we quantified genetic structure and color and pattern variation across three closely related species, Mantella aurantiaca, Mantella crocea, and Mantella milotympanum. Although our restriction site‐associated DNA (RAD) sequencing approach identified clear genetic clusters, they do not align with current species designations, which has important conservation implications for these imperiled frogs. Moreover, our results suggest that levels of intraspecific color variation within this group have been overestimated, while species diversity has been underestimated. Within major genetic clusters, we observed distinct patterns of variation including: populations that are phenotypically similar yet genetically distinct, populations where phenotypic and genetic breaks coincide, and populations that are genetically similar but have high levels of within‐population phenotypic variation. We also detected admixture between two of the major genetic clusters. Our study suggests that several mechanisms—including hybridization, selection, and drift—are contributing to phenotypic diversity. Ultimately, our work underscores the need for a reevaluation of how polymorphic and polytypic populations and species are classified, especially in aposematic organisms.     

DIFFERENCES IN THE REGULATION OF GROWTH AND BIOMINERALIZATION GENES REVEALED THROUGH LONG‐TERM COMMON‐GARDEN ACCLIMATION AND EXPERIMENTAL GENOMICS IN THE PURPLE SEA URCHIN

Across heterogeneous landscapes, populations may have adaptive differences in gene regulation that adjust their physiologies to match local environments. Such differences could have origins in acclimation or in genetically fixed variation between habitats. Here we use common‐garden experiments to evaluate differences in gene expression between populations of the purple sea urchin, Strongylocentrotus purpuratus, spanning 1700 km and average temperature differences of 5°C to 8°C. Across expression profiles from 18,883 genes after 3 years of common conditions, we find highly correlated expression patterns (Pearson's r = 0.992) among most genes. However, 66 genes were differentially expressed, including many ribosomal protein and biomineralization genes, which had higher expression in urchins originally from the southern population. Gene function analyses revealed slight but pervasive expression differences in genes related to ribosomal function, metabolism, transport, “bone” development, and response to stimuli. In accord with gene expression patterns, a post‐hoc spine regrowth experiment revealed that urchins of southern origin regrew spines at a faster rate than northern urchins. These results suggest that there may be genetically controlled, potentially adaptive differences in gene regulation across habitats and that gene expression differences may be under strong enough selection to overcome high, dispersal–mediated gene flow in this marine species.     

POPULATION GENETICS OF SKELETONEMA COSTATUM (BACILLARIOPHYCEAE) IN NARRAGANSETT BAY1

During a two year period 457 clones of the diatom Skeletonema costatum were isolated prior to and during the summer-fall and winter-spring blooms of this species in Narragansett Bay, R.I. Their allozyme banding patterns were examined for 5 enzyme loci. Genotypic frequencies indicated that the winter bloom populations were genetically different from the prevalent summer bloom populations of the same species. Genetic differences between seasonal blooms are as great as those found between species of terrestrial organisms, but are not accompanied by morphological variation. Although blooms have distinct prevalent forms, they are not genetically homogeneous. No single clone is ever representative of all populations of S. costatum. The dynamics of these allochronic populations appear to be governed by a form of cyclic natural selection, and are probably a regular feature of the cycles of abundance of this species in this area. These results cast doubt on some of the assumptions often made in the “autecological approach” to phytoplankton ecology. This study comprises the first quantitative examination of the population genetics of a microalga.     

GENETIC CONSTRAINTS ON MACROEVOLUTION: THE EVOLUTION OF HOST AFFILIATION IN THE LEAF BEETLE GENUS OPHRAELLA

We hypothesize that the evolution of an ecologically important character, the host associations of specialized phytophagous insects, has been influenced by limitations on genetic variation. Using as a historical framework a phylogenetic reconstruction of the history of host associations in the beetle genus Ophraella (Chrysomelidae), we have employed quantitative-genetic methods to screen four species for genetic variation in larval survival, oviposition (in one species only), and feeding responses to their congeners' host plants, in the Asteraceae. We here report results of studies of one species and evaluate the results from all four. Analysis of half-sib/full-sib families and of progenies of wild females of O. notulata, a specialist on Iva (Ambrosiinae), provided evidence of genetic variation in larval consumption of five of six test plants and in adult consumption of four of six. Larval mortality was complete on five plants; only on Ambrosia, a close relative of the natural host, was there appreciable, and genetically variable, survival. Oviposition on Ambrosia showed marginally significant evidence of genetic variation; a more distantly related plant elicited no oviposition at all. In compiling results from four Ophraella species, reported in this and two other papers, we found no evidence of genetic variation in 18 of 39 tests of feeding responses and 14 of 16 tests of larval survival on congeners' hosts. This result is consistent with the hypothesis that absence or paucity of genetic variation may constrain or at least bias the evolution of host associations. The lower incidence of genetic variation in survival than in feeding behavior may imply, according to recent models, that avoidance is a more common evolutionary response to novel plants than adaptation. The usually great disparity between mean performance on congeners' hosts and the species' natural hosts, and an almost complete lack of evidence for negative genetic correlations, argue against the likelihood that speciation has occurred by sympatric host shift. The presence versus apparent absence of genetic variation in consumption was correlated with the propinquity of relationship between the beetle species tested and the species that normally feeds on the test plant, suggesting that the history of host shifts in Ophraella has been guided in part by restrictions on genetic variation. It was also correlated with the propinquity of relationship between a test plant and the beetle's natural host. The contributions of plant relationships and insect relationships, themselves correlated in part, to the pattern of genetic variation, are not readily distinguishable, but together accord with phylogenetic evidence that these and other phytophagous insects adapt most readily to related plants. In this instance, therefore, the macroevolution of an ecologically important character appears to have been influenced by genetic constraints. We hypothesize that absence of the structural prerequisites for genetic variation in complex characters may affect genetic variation and the trajectory of evolution.     

CLINES IN CUTICULAR HYDROCARBONS IN TWO DROSOPHILA SPECIES WITH INDEPENDENT POPULATION HISTORIES

We took a comparative approach utilizing clines to investigate the extent to which natural selection may have shaped population divergence in cuticular hydrocarbons (CHCs) that are also under sexual selection in Drosophila. We detected the presence of CHC clines along a latitudinal gradient on the east coast of Australia in two fly species with independent phylogenetic and population histories, suggesting adaptation to shared abiotic factors. For both species, significant associations were detected between clinal variation in CHCs and temperature variation along the gradient, suggesting temperature maxima as a candidate abiotic factor shaping CHC variation among populations. However, rainfall and humidity correlated with CHC variation to differing extents in the two species, suggesting that response to these abiotic factors may vary in a species‐specific manner. Our results suggest that natural selection, in addition to sexual selection, plays a significant role in structuring among‐population variation in sexually selected traits in Drosophila.     

INCIPIENT SPECIATION BY SEXUAL ISOLATION IN DROSOPHILA MELANOGASTER: VARIATION IN MATING PREFERENCE AND CORRELATION BETWEEN SEXES

Genetic divergence for characters pertaining to reproductive isolation is of considerable interest in evolutionary biology. Since most studies concentrate on sibling species (for recent reviews, see Wu et al. 1996), we would like to know how much genetic variation exists between populations that are at an incipient stage of speciation. To answer this question, we have begun measuring variations in mating preference among natural isolates of Drosophila melanogaster, represented by the cosmopolitan and Zimbabwe sexual races. We quantify the variation in mating preference and success in both sexes by using a multiple-choice design and an index that is suited to cases of strong asymmetry in mate choice. Different designs and indices for measuring sexual isolation are also discussed. These sexual traits are entirely genetically determined. Surveying four populations in southern Africa and additional cosmopolitan lines, we observe extensive genetic variation in sexual characters as well as strong correlation between sexes. The populations are highly differentiated and represent various stages of evolution between the African and the cosmopolitan type of sexual behaviors. The genetic variation and correlation for these sexual characters coupled with their geographical pattern have interesting implications for models of speciation by sexual selection.     

EVOLUTION OF AN APHID-PARASITOID INTERACTION: VARIATION IN RESISTANCE TO PARASITISM AMONG APHID POPULATIONS SPECIALIZED ON DIFFERENT PLANTS

The evolution of associations between herbivorous insects and their parasitoids is likely to be influenced by the relationship between the herbivore and its host plants. If populations of specialized herbivorous insects are structured by their host plants such that populations on different hosts are genetically differentiated, then the traits affecting insect-parasitoid interactions may exhibit an associated structure. The pea aphid (Acyrthosiphon pisum) is a herbivorous insect species comprised of genetically distinct groups that are specialized on different host plants (Via 1991a, 1994). Here, we examine how the genetic differentiation of pea aphid populations on different host plants affects their interaction with a parasitoid wasp, Aphidius ervi. We performed four experiments. (1) By exposing pea aphids from both alfalfa and clover to parasitoids from both crops, we demonstrate that pea aphid populations that are specialized on alfalfa are successfully parasitized less often than are populations specialized on clover. This difference in parasitism rate does not depend upon whether the wasps were collected from alfalfa or clover fields. (2) When we controlled for potential differences in aphid and parasitoid behavior between the two host plants and ensured that aphids were attacked, we found that pea aphids from alfalfa were still parasitized less often than pea aphids from clover. Thus, the difference in parasitism rates is not due to behavior of either aphids or wasps, but appears to be a physiologically based difference in resistance to parasitism. (3) Replicates of pea aphid clones reared on their own host plant and on a common host plant, fava bean, exhibited the same pattern of resistance as above. Thus, there do not appear to be nutritional or secondary chemical effects on the level of physiological resistance in the aphids due to feeding on clover or alfalfa, and therefore the difference in resistance on the two crops appears to be genetically based. (4) We assayed for genetic variation in resistance among individual pea aphid clones collected from clover fields and found no detectable genetic variation for resistance to parasitism within two populations sampled from clover. This is in contrast to Henter and Via's (1995) report of abundant genetic variation in resistance to this parasitoid within a pea aphid population on alfalfa. Low levels of genetic variation may be one factor that constrains the evolution of resistance to parasitism in the populations of pea aphids from clover, leading them to remain more susceptible than populations of the same species from alfalfa.     

EVIDENCE FOR SELECTION ON A CHORDATE HISTOCOMPATIBILITY LOCUS

Allorecognition is the ability of an organism to differentiate self or close relatives from unrelated individuals. The best known applications of allorecognition are the prevention of inbreeding in hermaphroditic species (e.g., the self‐incompatibility [SI] systems in plants), the vertebrate immune response to foreign antigens mediated by MHC loci, and somatic fusion, where two genetically independent individuals physically join to become a chimera. In the few model systems where the loci governing allorecognition outcomes have been identified, the corresponding proteins have exhibited exceptional polymorphism. But information about the evolution of this polymorphism outside MHC is limited. We address this subject in the ascidian Botryllus schlosseri, where allorecognition outcomes are determined by a single locus, called FuHC (Fusion/HistoCompatibility). Molecular variation in FuHC is distributed almost entirely within populations, with very little evidence for differentiation among different populations. Mutation plays a larger role than recombination in the creation of FuHC polymorphism. A selection statistic, neutrality tests, and distribution of variation within and among different populations all provide evidence for selection acting on FuHC, but are not in agreement as to whether the selection is balancing or directional.     

Molecular Population Genetics of Rice Domestication

Domestication is a selection process that genetically modifies species to meet human needs. A most intriguing feature of domestication is the extreme phenotypic diversification among breeds. What could be the ultimate source of such genetic variations? Another notable outcome of artificial selection is the reduction in the fitness of domesticated species when they live in the wild without human assistance. The complete sequences of the two subspecies of rice cultivars provide an opportunity to address these questions. Between the two subspecies, we found much higher rates of non‐synonymous (N) than synonymous (S) substitutions and the N/S ratios are higher between cultivars than between wild species. Most interestingly, substitutions of highly dissimilar amino acids that are deleterious and uncommon between natural species are disproportionately common between the two subspecies of rice. We suggest strong selection in the absence of effective recombination may be the driving force, which we called the domestication‐associated Hill‐Robertson effect. These hitchhiking mutations may contribute to some fitness reduction in cultivars. Comparisons of the two genomes also reveal the existence of highly divergent regions in the genomes. Haplotypes in these regions often form highly polymorphic linkage blocks that are much older than speciation between wild species. Genes from such regions could contribute to the differences between indica and japonica and are likely to be involved in the diversifying selection under domestication. Their existence suggests that the amount of genetic variation within the single progenitor species Oryza rufipogon may be insufficient to account for the variation among rice cultivars, which may come from a more inclusive gene pool comprising most of the A‐genome wild species. Genes from the highly polymorphic regions also provide strong support for the independent domestication of the two subspecies. The genomic variation in rice has revealing implications for studying the genetic basis of indica‐japonica differentiation under rice domestication and subsequent improvement.