VARIATION IN PREFERENCE AND SPECIFICITY IN MONOPHAGOUS AND OLIGOPHAGOUS SWALLOWTAIL BUTTERFLIES

Although variation in oviposition preference and specificity for host plants has been demonstrated within populations of a variety of oligophagous insect species, it is unknown whether genetic variation in host choice is lost within populations of monophagous species. Analysis of a locally monophagous butterfly species, Papilio oregonius, and a locally oligophagous species, P. zelicaon, showed significant variation in oviposition preference within populations of both species. Females of both species chose primarily their native hosts. Nonetheless, the percentages of eggs laid by individual females among the plant species and the number of plant species on which individual females laid eggs differed significantly among isofemale strains within populations. Moreover, some females within all isofemale strains of both species laid a few eggs on Foeniculum vulgare, an umbelliferous species that does not occur in the native habitats of these populations but is a host for Papilio species in other geographic areas. The results suggest that local monophagy and oligophagy in these species reflect the relative ranking among potential plant species. Both populations harbor variation in oviposition choice that could allow for host shifts if these populations invaded new habitats.     

PREFERENCE HIERARCHIES AND THE ORIGIN OF GEOGRAPHIC SPECIALIZATION IN HOST USE IN SWALLOWTAIL BUTTERFLIES

Four allopatric populations of the widely distributed western anise swallowtail butterfly, Papilio zelicaon, use different plant genera as hosts, but simultaneous choice experiments showed that these populations have diverged only slightly in oviposition preference. Of the four populations—two from southeastern Washington State, one from coastal southwestern Washington State, and one from central California—three use hosts that are not available to any of the others. Although variation for the degree of preference for particular plant species occurred within and among populations, all four populations ranked hosts in the same overall order. Monophagy on a local, low-ranking host outside the range of high-ranking hosts did not necessarily lead to the loss of preference for those high-ranking hosts, thereby indicating that the high-ranking hosts would still be accepted, and in some cases even preferred, if a population encountered them again. Hence, the overall preference hierarchy among P. zelicaon populations appears to be evolutionarily conservative. Analyses of differences among families within the California population indicated that increased preference for some hosts is inversely correlated, whereas preference for other hosts may be uncorrelated. Positive correlations may also occur but were not observed among the plant species tested. Overall, the results indicate local monophagy on different plant species in P. zelicaon has not involved major reorganizations in the preference hierarchy of ovipositing females, even in populations that may have fed on a low-ranking host for many generations. Instead, small increases in preference for local hosts have occurred within an evolutionarily conservative preference hierarchy.     

THE DIVERSITY AND EVOLUTION OF BATESIAN MIMICRY IN PAPILIO SWALLOWTAIL BUTTERFLIES

Papilio swallowtail butterflies exhibit a remarkable diversity of Batesian mimicry, manifested in several sex-limited and polymorphic types. There is little understanding of how this diversity is distributed within Papilio , and how different mimicry types have evolved in relation to each other. To answer these questions, I present a graphical model that connects various mimicry types by hypothetical character state changes within a phylogenetic framework. A maximum likelihood analysis of evolution of mimicry types on the Papilio phylogeny showed that sexually monomorphic mimicry and female-limited mimicry have evolved repeatedly but predominantly independently in different clades. However, transitions between these mimicry types are rarely observed. The frequency distribution of character state changes was skewed in favor of the evolution of mimicry, whereas many theoretically plausible character state changes, especially evolutionary loss of mimicry, were not evident. I discuss these findings in relation to studying the tempo of evolutionary change, loss of traits, and directionality and connectivity among character states. The pathway approach and phylogenetic patterns of mimicry demonstrated in Papilio are useful to test novel hypotheses regarding the diversity and evolutionary directionality of Batesian mimicry in other systems.     

GENETICS OF MIMICRY IN THE TIGER SWALLOWTAIL BUTTERFLIES,PAPILIO GLAUCUS AND P. CANADENSIS (LEPIDOPTERA: PAPILIONIDAE)

The tiger swallowtail butterfly, Papilio glaucus, exhibits a female-limited polymorphism for Batesian mimicry; the Canadian tiger swallowtail, Papilio canadensis, lacks the mimetic (dark) form entirely. The species hybridize to a limited extent where their ranges overlap. Field collections and censuses indicate that mimetic females occur throughout the range of P. glaucus but at lowest frequencies in populations at the latitudinal edges of its geographic range such as the southernmost part of Florida and along the entire northern edge of its distribution from Massachusetts to Minnesota. Frequencies of mimetic females have remained relatively stable over time. Inheritance of the mimetic form is controlled primarily by two interacting sex-linked loci. The typical matrilineal pattern of inheritance in P. glaucus can be explained by polymorphism at a Y-linked locus, b. Analysis of P. glaucus × P. canadensis crosses has also revealed an X-linked locus, s, which controls the expression of the mimetic phenotype. The P. canadensis allele, s^can, suppresses the mimetic phenotype in hybrid and backcross females. Results from more than 12 yr of rearing tiger swallowtails, including interspecies hybrids, indicate that the absence of mimetic P. canadensis females is due to both a high frequency of the “suppressing” allele s^can and low frequency of the black-pigment-determining b + allele. The frequency of s^can (or other suppressing alleles of s) in P. glaucus populations outside the hybrid zone is low. Some males heterozygous at the s locus and some suppressed mimetic females occur within the hybrid zone. A simple genetic model predicts the frequency of daughters that differ in phenotype from their mothers.     

THE EVOLUTIONARY GENETICS OF MALE LIFE-HISTORY CHARACTERS IN DROSOPHILA MELANOGASTER

Alternative models of the maintenance of genetic variability, theories of life-history evolution, and theories of sexual selection and mate choice can be tested by measuring additive and nonadditive genetic variances of components of fitness. A quantitative genetic breeding design was used to produce estimates of genetic variances for male life-history traits in Drosophila melanogaster. Additive genetic covariances and correlations between traits were also estimated. Flies from a large, outbred, laboratory population were assayed for age-specific competitive mating ability, age-specific survivorship, body mass, and fertility. Variance-component analysis then allowed the decomposition of phenotypic variation into components associated with additive genetic, nonadditive genetic, and environmental variability. A comparison of dominance and additive components of genetic variation provides little support for an important role for balancing selection in maintaining genetic variance in this suite of traits. The results provide support for the mutation-accumulation theory, but not the antagonistic-pleiotropy theory of senescence. No evidence is found for the positive genetic correlations between mating success and offspring quality or quantity that are predicted by “good genes” models of sexual selection. Additive genetic coefficients of variation for life-history characters are larger than those for body weight. Finally, this set of male life-history characters exhibits a very low correspondence between estimates of genetic and phenotypic correlations.     

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.     

VARIATION IN OVIPOSITION PREFERENCE OF HELIOTHIS VIRESCENS IN RELATION TO MACROEVOLUTIONARY PATTERNS OF HELIOTHINE HOST RANGE

When cotton, geranium, petunia, tobacco, tomato, and velvetleaf were presented simultaneously to strains of the Heliothine moth, Heliothis virescens (F.), from Arizona (AZ), Mississippi (MS), and North Carolina (NC), oviposition choices were similar, while a strain from the Virgin Islands (VI) was significantly different from both the AZ and MS strains. In the MS-VI six-host test, the VI strain laid a higher proportion of its eggs on tomato and a lower proportion of its eggs on petunia than did the MS strain. Since petunia and tomato are in the same plant family (Solanaceae), differences between the strains in host preference do not appear to involve traits common to all members of a plant family. In the AZ-VI six-host test, the AZ strain laid a higher percentage of its eggs on tobacco and lower percentages on geranium and velvetleaf (Malvaceae) than did the VI strain. The percentages of eggs laid on cotton (Malvaceae) by the two strains were not significantly different. When moths were placed in cages with only tobacco and geranium, the AZ strain again laid a higher percentage of its eggs on tobacco than did the VI strain. However, when host choice was restricted to tobacco and cotton or velvetleaf and cotton, no significant difference between strains was found. Reciprocal hybrids of the AZ and VI strains were intermediate to the parental stocks in their preference for tobacco over geranium, indicating that a genetic mechanism was responsible for oviposition preference. The relevance of these findings to seemingly rapid fluxes in host range among members of the Heliothinae is discussed.     

DEVELOPMENT,FUNCTION, AND THE QUANTITATIVE GENETICS OF WING MELANIN PATTERN IN PIERIS BUTTERFLIES

Do genetic correlations among phenotypic characters reflect developmental organization or functional coadaptation of the characters? We test these hypotheses for the wing melanin pattern of Pieris occidentalis butterflies, by comparing estimated genetic correlations among wing melanin characters with a priori predictions of the developmental organization and the functional (thermoregulatory) organization of melanin pattern. There were significant broad-sense heritabilities and significant genetic correlations for most melanin characters. Matrix correlation tests revealed significant agreement between the observed genetic correlations and both developmental and functional predictions in most cases; this occurred even when the overlap between developmental and functional predictions was eliminated. These results suggest that both developmental organization and functional coadaptation among melanin characters influence the genetic correlation structure of melanin pattern in this species. These results have two important implications for the evolution of melanin pattern in P. occidentalis and other butterflies: 1) most phenotypic variation in pattern may reflect variation among, rather than within, sets of developmentally homologous wing melanin characters; and 2) in a changing selective environment, genetic correlations may retard the disruption of functionally coupled melanin characters, thus affecting the evolutionary response to selection.     

MITOCHONDRIAL DNA VARIATION WITHIN AND BETWEEN SPECIES OF THE PAPILIO MACHAON GROUP OF SWALLOWTAIL BUTTERFLIES

Species limits and phylogenetic relationships in the Papilio machaon species group are potentially confounded by a complex pattern of Pleistocene range fragmentation, hybridization, and ecological race formation. Mitochondrial DNA (mtDNA) restriction-site analysis has been used to define genetic affinities and genetic population structure within this species group. The distribution of mtDNA haplotypes generally confirms prior phylogenetic hypotheses and species delineations, but there is poor correspondence between ecological races and mtDNA haplotypes. The amount and distribution of mtDNA sequence variation within species vary among species, reflecting differences in current patterns of gene flow and/or historical population structure. In spite of wing pattern characters that ally them with P. polyxenes, both P. joanae and P. brevicauda have mtDNA that is closely related to that of P. machaon. We suggest that P. joanae and P. brevicauda are of hybrid origin.     

GENETIC COVARIANCE BETWEEN OVIPOSITION PREFERENCE AND LARVAL PERFORMANCE IN AN INSECT HERBIVORE

An experimental study determined that females of the herbivorous fly species Liriomyza sativae (Diptera: Agromyzidae) preferentially oviposit on the plant species on which their female progeny attain the greatest pupal weight. A modified parent/offspring regression was used to quantify this relationship as an additive genetic covariance between host-plant preference and relative performance of female larvae on different plant species. The implications of a genetic covariance between preference and performance on the course of evolution in herbivores are discussed. Several females from one population refused to oviposit on one of the plant species; this population also suffered the only significant larval mortality on this plant. These results corroborate the avoidance of unsuitable host plants seen in the genetic analyses of individuals, but relative to the genetic data, such population-level data are of limited usefulness in the study of evolutionary mechanisms by which insect populations become adapted to their host plants.     

CONNECTING QTLS TO THE G-MATRIX OF EVOLUTIONARY QUANTITATIVE GENETICS

Evolutionary quantitative genetics has recently advanced in two distinct streams. Many biologists address evolutionary questions by estimating phenotypic selection and genetic (co)variances ( G matrices). Simultaneously, an increasing number of studies have applied quantitative trait locus (QTL) mapping methods to dissect variation. Both conceptual and practical difficulties have isolated these two foci of quantitative genetics. A conceptual integration follows from the recognition that QTL allele frequencies are the essential variables relating the G -matrix to marker-based mapping experiments. Breeding designs initiated from randomly selected parental genotypes can be used to estimate QTL-specific genetic (co)variances. These statistics appropriately distill allelic variation and provide an explicit population context for QTL mapping estimates. Within this framework, one can parse the G -matrix into a set of mutually exclusive genomic components and ask whether these parts are similar or dissimilar in their respective features, for example the magnitude of phenotypic effects and the extent and nature of pleiotropy. As these features are critical determinants of sustained response to selection, the integration of QTL mapping methods into G -matrix estimation can provide a concrete, genetically based experimental program to investigate the evolutionary potential of natural populations.     

INTRASEXUAL SELECTION CONSTRAINS THE EVOLUTION OF THE DORSAL COLOR PATTERN OF MALE BLACK SWALLOWTAIL BUTTERFLIES,PAPILIO POLYXENES

Males of the eastern black swallowtail (Papilio polyxenes asterius Stoll) with typical coloration were more successful in intrasexual competition for mating territories than were males altered to have female-like mimetic coloration. Sibling males were matched for wingspan and emergence date and released as pairs, one with its pattern altered and one a control that was marked but with unaltered appearance. Significantly fewer altered males were resighted one or more days after release compared with control males (33% vs. 76%, 1990; 46% vs. 83%, 1993). Altered males were less able to establish and maintain themselves in preferred territories. The inability of released, altered males to establish a territory appears related to significantly longer male-male encounters. Encounters involving at least one participant with altered appearance averaged 66 s compared with 24 s if neither male was altered. However, altering the coloration of P. polyxenes males that already had established themselves in a territory had little effect. After courtships of similar duration (≈ 40 s), released virgin females were equally likely to mate with either altered or control males. This suggests that male-male intrasexual selection is of greater importance than female mate choice in maintaining a non-mimetic dorsal coloration in male P. polyxenes.