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Genetics of mimicry in the tiger swallowtail butterflies, Papilio glaucus and P. canadensis (Lepidoptera: Papilionidae)

The tiger swallowtail butterfly, Papilio glaucus L. (Lepidoptera: Papilionidae) exhibits a female-limited polymorphism for Batesian mimicry of the pipevine swallowtail, Battus philenor (L.) (Edwards 1884; Poulton 1909; J. Brower 1958). In males and nonmimetic ("yellow morph") females, the background color on wings and body is produced by yellow scales. In mimetic ("dark morph") females, the yellow pigment is replaced by a dark brown or black; the black bars that create the tiger stripe pattern of nonmimetic P. glaucus are not altered and remain visible as a fainter pattern against the background [ILLUSTRATION FOR FIGURE 1 OMITTED]. The mimetic form does not occur in the Canadian tiger swallowtail, Papilio canadensis R and J, a closely related species that occupies a largely parapatric range to the north of P. glaucus (Hagen et al. 1991; Opler 1992).

The genetic basis of the color polymorphism in P. glaucus was the subject of extensive studies by Clarke and Sheppard (1959, 1962), who concluded that dark background color is determined by a Y-(W-) linked gene. Y-linkage of the background-color determining locus (b) explains the observations that dark males are never produced and that dark morph females usually produce only dark daughters, whereas yellow morph females usually produce only yellow daughters. Efforts to analyze this Y-linked trait in more detail have been unsuccessful: an apparent association with heterochromatic polymorphism in P. glaucus (Clarke et al. 1976) was not supported in subsequent studies (Cross and Gill 1979).

Occasionally, dark-morph P. glaucus females will produce yellow daughters and, more rarely, yellow morph females will produce dark daughters. These exceptions to strict matrilineal inheritance of the mimetic phenotype were noted by Clarke and Sheppard (1962) as well as by earlier naturalists (Edwards 1884). Chromosomal abnormalities have been suggested as explanations for some of these cases (Clarke and Sheppard 1962; Clarke and Clarke 1983; Scriber and Evans 1986).

Scriber et al. (1987) proposed an alternative explanation, based on their discovery of a dark morph "suppressor" in P. canadensis. They argued that presence of a suppressor at low frequency in P. glaucus populations could account for many of these exceptions. Genes for suppression might be introduced through natural hybridization with P. canadensis, considered at the time to be a subspecies of P. glaucus. They predicted that exceptions to matrilineal inheritance would be more frequent in P. glaucus populations closer to the hybrid zone than in those further away.

In subsequent studies, X-(Z-) linkage of the P. canadensis suppressor gene, [s.sup.can], was demonstrated by analysis of back-cross progeny from interspecies crosses (Hagen and Scriber 1989). Genetic mapping of the X chromosome revealed that [s.sup.can] is closely linked to the 6-Phosphogluconate dehydrogenase (Pgd) locus, and to another P. canadensis gene, [od.sup.can] which appears to be responsible for "obligate" diapause in P. canadensis (Rockey et al. 1987; Hagen and Scriber 1989), The [s.sup.can] gene does not appear to have any phenotypic effect on males or yellow-morph females. However, the evolutionary role of such a suppressor is puzzling. Preliminary evidence suggested that P. canadensis females lacked the dark-pigment-determining allele b+ (Scriber et al. 1987). Perhaps [s.sup.glau] should be viewed as an "enabler" of b+ in P. glaucus.

The 12 possible combinations of paternal and maternal genotypes for the s and b loci and the resulting genotypes and phenotypes of the female ofspring are summarized in Table 1. Only four combinations result in female-offspring phenotypes that differ from the mother's. An important prediction from this simple two-locus model is that the two combinations that result in both dark and yellow female offspring from a single mother both give an expected 1:1 ratio of female-offspring phenotypes, assuming that sperm from only one male has fertilized the eggs (Thornhill and Alcock 1983; Drummond 1984).

This model also enables simple predictions about the frequency of exceptional family types, assuming that mating is random with respect to suppressor phenotype, selection is weak, and allele frequencies in males and females are equal (Table 1). The expected overall frequency of females producing female offspring unlike themselves, from a sample of [TABULAR DATA FOR TABLE 1 OMITTED] mated females collected from a P. glaucus population, is 3bs (1 - s), where b is the frequency of the dark-pigment determining allele b+ and s is the frequency of the suppressor [s.sup.can]. The four individual types of exceptions are yellow mother, dark female offspring; yellow mother, dark and yellow female offspring; dark mother, dark and yellow female offspring; and dark mother, yellow female offspring. The expected proportion of female offspring unlike their mothers is 2bs (1 - s) because only one-half of the female offspring from two of these categories of exceptions are unlike their mothers.

An independent estimate of the frequency of s alleles can be obtained by hand pairing field collected males with dark-morph females and recording their female offspring's phenotypes. Males that sire both yellow and dark female offspring from a single dark female may be inferred to be heterozygous for the suppressor; whereas those siring only dark or yellow female offspring may be inferred to be homozygous for nonsuppressing ([s.sup.glau]) or suppressing ([s.sup.can]) alleles, respectively. (Female offspring inherit their single X chromosome from the males only.) Additional test crosses might be used as well to infer genotypes; however, the greatly increased time and labor required, and rearing mortality, severely limit the sample sizes achievable in practice.

In addition to dark and yellow morphs, female P. glaucus of intermediate ("sooty") color occur. We have collected or reared such intermediate females from numerous locations, and additional field collections have been reported from virtually every state from Florida northward to Wisconsin (Edwards 1884; Clark 1932; Clark and Clark 1951; Harris 1972; Scriber et al. 1987). Some cases may be attributable to additional modifiers at the s or unknown (autosomal?) loci (Clarke et al. 1976; Clarke and Willig 1977; Scriber et al. 1990). Environmental conditions during larval or pupal development also affect adult color (Ritland 1986; W. Bergman, pers. comm., 1982). Females with intermediate colors have been shown to be temperature sensitive, with a greater proportion of female offspring from dark mothers exhibiting intermediacy when reared at high temperatures (Ritland 1986).

The occurrence of intermediate females and reports of patterns of inheritance that could not be explained fully by segregation of a single X-linked suppressor allele (Scriber and Evans 1986; Hagen and Scriber 1989; Scriber et al. 1990) indicated the need to examine a larger number of families to assess the adequacy of our present genetic understanding of mimicry in tiger swallowtails. If "inexplicable" cases constitute a large fraction of the exceptions to strict matrilineal inheritance, more complex models may be required (e.g., Blanchard and Descimon 1988; Nijhout 1991).

In this report, we summarize field collection and census records for P. glaucus populations to estimate the geographic range of occurrence of the mimetic dark-morph phenotype and its frequency over repeated censuses in several populations. Results from 12 yr (1980-1992) of rearing P. glaucus, P. canadensis, and hybrids in our laboratory are analyzed to address the following questions: (1) How frequent are cases of nonmatrilineal inheritance of mimetic phenotype in tiger swallowtails? (2) Does the two-locus (s and b) model adequately account for observed patterns of inheritance of mimetic phenotype? (3) If so, what are the frequencies of s and b alleles in P. glaucus and P. canadensis populations?

MATERIALS AND METHODS

Our laboratory-rearing studies were conducted under controlled-environment conditions during 1980-1986 in Madison, Wisconsin, and during 1987-1992 in East Lansing, Michigan, using stocks of tiger swallowtail butterflies from sites located from central Florida and Texas to Alaska, Alberta, Manitoba, and Ontario. Butterflies for these experiments were offspring of field-captured females that had mated naturally with unknown males in the field, or of laboratory-reared females that were hand-paired to males of known background.

Mated females were induced to oviposit on food plant leaves supported in water-filled rubber-capped plastic vials in clear plastic boxes (12 x 20 x 30 cm) under heat from incandescent lightbulbs placed at a distance of 0.3-0.5 m away. The eggs produced were collected at two-day intervals until each female died, and fertility and viability were recorded for each female (Lederhouse and Scriber 1987a). Larvae were kept in 4 x 15 cm diameter plastic petri dishes with screened ventilation, generally in groups of 4-5 siblings and maintained on a 16:8 h photo:scotophase cycle with a corresponding temperature cycle of 23.5 [degrees] C: 19.5 [degrees] C in Wisconsin (and at 18:6 h and 24 [degrees] C in Michigan subsequent to 1986). They were supplied with fresh excised leaves that were kept turgid by use of water-filled vials and changed as needed. Most larvae were reared entirely on black cherry foliage (Prunus serotina Ehrh.). In some cases, larvae were transferred to black cherry from other plant species following the completion of the first instar. Larvae were individually removed from dishes as prepupae. Pupae were weighed after two days and placed in cylindrical screen cages until adult eclosion.

All reared adults have been retained as voucher specimens in our research collection at Michigan State University. Each individual is coded by a number assigned to its mother when she was mated or collected and by a further individual code corresponding to its pupal mass (to 0.5 mg). Approximately 30,000 P. glaucus adults are included in the collection. Despite careful rearing techniques, a native larva on host-plant leaves could have been accidentally introduced and subsequently reared with an experimental test brood. Also, it is possible that some errors in classifying intermediates and recording individuals could have occurred and remained undetected. Although some might consider all cases of a single "exceptional" female offspring in a "normal" brood as a possible mistake, such unresolved exceptional cases involved only five individual females from four populations. One Ohio population produced repeatable exceptional cases every year (see also Scriber and Evans 1986, 1988a).

Dark and yellow morphs occurring in P. glaucus (and the Mexican P. alexiares) are the extremes of a continuum which goes from (1) yellow morph, to (2) lightly dusted or sooty yellow, (3) a perfect intermediate (see Scriber et al. 1987), (4) heavy-sooty coloration with underlying tiger pattern showing, and (5) the normal dark morph. This range of color variations is also illustrated in hybrids of dark P. glaucus and Papilio rutulus (Scriber et al. 1990).

A different series of color-blotched irregularities are termed mosaics and/or gynandromorphs (Scriber and Evans 1988a). Other aberrant color polymorphisms can be male limited (Scriber and Lintereur 1983) or female limited (Scriber and Evans 1988b; Scriber 1990a). Such aberrants are not included in our tables here, and we include only one "intermediate" category for all individuals with a color pattern between the two standard female morphs (yellow and dark). Methods for allozyme electrophoresis and scoring of banding patterns are described in Hagen and Scriber (1989, 1991).

Field and Museum Censuses

In addition to the Papilio we collected during the 1979-1994 seasons, the locations where dark-morph females (P. glaucus) had been collected were recorded from insect collections in various museums, universities, and private collections (see Acknowledgments). The museums included Allyn (FL), California Academy of Sciences, Carnegie (PA), Florida State Insect Collection, Los Angeles County Museum (CA), Milwaukee Public Museum (WI), and the Illinois Natural History Survey. The university insect collections included Cornell, Georgia State, Michigan State, Mississippi State, Pennsylvania State, University of California (Berkeley, Davis, and Riverside), University of Georgia (Athens), University of Illinois (Champaign), University of Kansas (Lawrence), University of Louisville (KY), University of Minnesota, University of Missouri (Columbia), and University of Wisconsin (Madison).

RESULTS

Distribution of Mimetic Females

Our collection data supplemented with museum records indicate high relative abundance of dark-morph females from the central and southern Appalachian Mountains extending westward to Texas [ILLUSTRATION FOR FIGURE 2 OMITTED]. The relative abundance of dark females decreases southward in peninsular Florida, eastward along the Atlantic coast, and northward along the entire hybrid zone with P. canadensis. Repeated collections at a variety of locations reveal surprisingly constant relative morph frequencies over the last decade or more (Table 2). One exception is Highlands County, Florida, where the mimetic morph has increased since 1960.

Intraspecific Crosses

During the study period, nearly all females produced female offspring the same color as themselves, in common with the results reported by Clarke and Sheppard (1959, 1962) and consistent with maternal (Y-linked or cytoplasmic) inheritance of female color. All 240 female P. canadensis collected from Alaska, Canada, northern Wisconsin, northern Michigan, northern New York, and central Vermont were yellow, and so were 972 of 973 female offspring reared (Table 3A). The single exception was a dark female offspring from a Marquette County (WI) female. Exceptional individuals (with female-offspring color unlike the mother) represented only 0.1% of all P. canadensis female offspring.

For 196 yellow-morph females of P. glaucus collected from Florida, Georgia, Illinois, Indiana, Kentucky, Louisiana, southern Michigan, New Jersey, Ohio, South Carolina, Texas, West Virginia, and southern Wisconsin, 997 of 1034 female offspring were yellow. Ten exceptional broods (= 5.1%) were observed (Table 3B). For 377 dark P. glaucus mothers from [TABULAR DATA FOR TABLE 2 OMITTED] the same states plus Tennessee and Virginia, 1948 of 1993 female offspring were dark. Nineteen exceptional broods (5.1%) were observed (Table 3C). Exceptional female offspring comprised 3.6% of the total female progeny of yellow-morph P. glaucus and 1.7% of the total female progeny of dark-morph P. glaucus females (Tables 3B-C).

Intraspecific pairings (N = 88) using field-collected P. glaucus males resulted in very few exceptional broods (Table 4). There were only 11 families in which at least one female offspring was of different color than her mother (Table 4). Two of these from southern Ohio may have been chromosomally abnormal mothers (Scriber and Evans 1986), and eight involved at least one parent from this same Ohio population. One dark female of six female offspring from a yellow Michigan female mated to a Michigan male represents the 11th exceptional family, unless this individual was accidentally introduced. In summary, exceptions to matrilineal inheritance are rare.

Interspecific Hybridization

Forty pairings of P. canadensis females to P. glaucus males were made. Dark femalr offspring were produced in only four [TABULAR DATA FOR TABLE 3A OMITTED] of these pairings. These particular pairings used Adams County (OH) glaucus males from a population which was known to contain an abnormality (Scriber and Evans 1986). In fact, 21 of the 24 odd segregants (from a total of 327 female offspring) are from a single brood (#1132). It is especially interesting that this involved the same individual male parent used also in pairing #1129, which also produced irregular results (i.e., odd color segregants; see Table 4). Sex ratios were nearly 1:1 in these P. canadensis x P. glaucus pairings (327 female; 297 male; 190 dead pupae, Hagen and Scriber 1995).

In contrast to intraspecific crosses, almost all female offspring of dark-morph P. glaucus females mated with P. canadensis males were yellow (of 823 female offspring, only 141 were dark and 59 were intermediate; Table 5). Except for a single intermediate female offspring from an Alaskan father, all cases in which dark or intermediate female offspring appeared were concentrated along the Great Lakes hybrid zone [ILLUSTRATION FOR FIGURE 3 OMITTED]. Populations with P. canadensis-type fathers, which resulted in some dark female offspring in these P. glaucus pairings include Barron, Marquette, Green Lake, [TABULAR DATA FOR TABLE 3B OMITTED] [TABULAR DATA FOR TABLE 3C OMITTED] and Wood counties in Wisconsin; Allegan, Newaygo, Livingston, Isabella, Ingham, Washtenaw, and Leelanau (South Manitou Island) counties in Michigan; and Tompkins County in central New York (Table 5).

One hybrid pairing (#1396) involved a virgin dark Texas glaucus and a putative canadensis male from Marquette County, Wisconsin (near the center of zone of hybrid interaction). A color range of [F.sub.1] hybrid female offspring from [TABULAR DATA FOR TABLE 4 OMITTED] [TABULAR DATA FOR TABLE 5 OMITTED] typical yellow through intermediate to dark was observed for this brood (Table 5; [ILLUSTRATION FOR FIGURE 4 OMITTED]). Even if the male was heterozygous for an X-linked suppressor (enabler), we might have expected a mix of typical dark and typical yellow female offspring but not so many intermediate types, where only partial suppression occurs. A population from adjacent Green Lake County yielded a dark female #1303 (Table 3C) that produced yellow and intermediate female offspring [ILLUSTRATION FOR FIGURE 5 OMITTED], which strengthens the suggestion that these represent hybrid populations with genetic introgression. Although we did not analyze allozyme frequencies, which could be diagnostic for these suspected hybrid Green Lake County and Marquette County populations (Hagen et al. 1991), the neonate (first instar) larval survival for offspring of female #1303 (which resulted in yellow and intermediate female offspring) was 100% on both quaking aspen, Populus tremuloides, and tuliptree, Liriodendron tulipifera. Such results also support the idea that these populations are indeed of hybrid origin with genetic introgression of the very distinct detoxification abilities of the two species for Salicaceae and Magnoliaceae (Scriber et al. 1989b).

Backcrosses using yellow P. glaucus (D) x P. canadensis hybrid females (with dark potential) paired with P. glaucus males resulted in a near total reexpression of dark color among female offspring (Table 6). Dark female offspring were observed in 31 of 32 families (the exceptional family consisted of only one female offspring). If suppression were completely reversible, all female offspring of these crosses should be dark. In these backcrosses, only 25 female offspring were yellow, whereas 423 female offspring were dark (or intermediate), which verifies that the suppressor effect from P. canadensis observed in the yellow mothers is largely reversible. Ten of the 25 yellow female offspring were from family #2509, sired by a male from West Virginia. This male was putatively a P. glaucus, however from a population close to the zone of suspected hybrid interaction with P. canadensis (see Hagen 1990; Scriber 1990b). The 50:50 dark:yellow segregation in family #2509 may have resulted if the male was heterozygous for the suppressor.

In contrast, glaucus (D) x canadensis hybrid females paired to male P. canadensis produced primarily yellow female offspring (N = 240 yellow, with only six intermediate or dark female offspring from 15 pairings; Table 7). The three exceptional broods with some dark female offspring had male parents that were from populations near the hybrid zone (in central Wisconsin). One [F.sub.2] pairing between a yellow female (glaucus (D) x canadensis) paired with a hybrid male exhibited a segregation of both dark and yellow female offspring (Table 8).

Sex Ratios and Segregating Color Patterns

Results from test crosses of P. canadensis males to dark-morph P. glaucus females were analyzed for sex ratios of offspring (Table 9). The simple two-locus model for female color predicts that the proportion of yellow female offspring in families with morphs segregating should be 50% (Table 1). That expectation was clearly not met (Table 9). Only families with both dark and intermediate morphs segregated at approximately 50%. However, all family groups produced fewer female than male offspring (Table 9), suggesting that deviations from the expected 50% ratio could be explained, in part, by selective mortality of females with particular X-chromosome genotypes. For example, 12 backcross pairings yielded 63 dark females, 34 yellow females, 133 males, and 37 dead pupae. This skewness may reflect differential mortality or extended diapause for yellow female offspring. In fact, ecdysone injections in pupae of brood #4260 brought out 21 yellow females, four dark females, and 22 males the following year (Hagen and Scriber 1989). If the 37 dead pupae in the 12 backcrosses were all or mostly yellow females, the ratio of dark:yellow would be very close to 1:1, as predicted by the simple single X-linked suppressor allele.

The occurrence of families with all three morphs (yellow, intermediate, and dark) was also unexpected based on the simple two-locus genetic model. One such family, #3770, sired by a male from Tompkins County (NY) had seven yellow, five intermediate, and 14 dark female offspring (Table 5). Twenty-five of these offspring were analyzed by allozyme electrophoresis and scored for X-linked genotypes using techniques described previously (Hagen and Scriber 1989; Hagen 1990; Hagen et al. 1991). Although the seven yellow female offspring had the [Pgd.sup.-140] allele, 18 of the dark and intermediate female offspring had the [Pgd.sup.-100] allele (one dark female offspring was not scored). Increased mortality of suppressed females may also explain the smaller number of yellow female offspring in this odd New York brood (#3770) and the smaller number of [Pgd.sup.-140] relative to [Pdg.sup.-100] alleles.

Three aspects of these data are significant: the Pgd locus is closely linked to the s locus (Hagen and Scriber 1989), the [Pgd.sup.-100] allele is the common P. glaucus allele, and Tompkins County lies within the hybrid zone between P. glaucus and P. canadensis (Hagen 1990). These results imply that (1) the sire of family #3770 was heterozygous for suppressing/nonsuppressing s alleles (as well as heterozygous for [Pgd.sup.-100/Pgd-140]); [TABULAR DATA FOR TABLE 6 OMITTED] (2) yellow female offspring inherited the suppressing allele; and (3) dark and intermediate morphs represent phenotypic variation within the nonsuppressed genotype. None of the other segregating families thus far examined has had segregating X-linked marker alleles.

DISCUSSION

Relative Abundance of Mimetic Females

Papilio glaucus dark-morph females occur from southern Florida and central Texas northward to the Great Lakes hybrid zone (central Minnesota to Massachusetts; [ILLUSTRATION FOR FIGURE 2 OMITTED]). Although we examined extensive personal and museum collections, many counties where dark-morph females are likely to occur lack specimen records for dark-morph females. This probably occurs because the dark form is so common in these states that it is frequently assumed to be throughout the state in question and consequently not collected or retained. For example, there are older reports that the dark-morph females are so abundant that yellow-morph females are assumed to be rare or absent from the states of Alabama and Mississippi (Mather 1954). To our knowledge, only a single yellow female P. glaucus from Mississippi and only one from Alabama have ever been reported (Mather and Mather 1958).

In contrast, at the northern range limits of P. glaucus, dark-morph females are rare and actively sought by lepidopterists. Lack of records for dark-morph females across the hybrid zone are much more likely to reflect true absences (Ebner 1970; Shapiro 1974). For example, intensive butterfly surveys of every county in Massachusetts from 1986-1990 failed to turn up even a single dark-morph P. glaucus female (Chris Leahy of the Massachusetts Audubon Society, pers. [TABULAR DATA FOR TABLE 7 OMITTED] comm., 1992). Furthermore, these northern limits to dark-morph distribution appear to have been relatively constant for at least the last century. Edwards (1884) reports that "north of a certain latitude, about 41 [degrees] 30 [minutes] on the Hudson River, and 42 [degrees] 30 [minutes] in Wisconsin, all the females are yellow." He does indicate that West Virginia (latitude 38 [degrees] N) seems to be an exception in that he finds yellow females there, "while they seem never so common as the black." We suggest that the Appalachian Mountains provide altitudinal refugia for canadensis types and that an inability to complete two generations may select against the X-linked glaucus genes much as in the Great Lakes hybrid zone (Scriber 1988, 1990b; Scriber and Lederhouse 1992). Thomas Allen (pers. comm., 1992) reports that the second generation P. glaucus flight in West Virginia is almost entirely dark females, whereas the first flight has many yellow females.

Careful observations for five years in the 1870s indicated 83-86% dark morphs in northern Illinois (Edwards 1884). Edwards (1884) also notes that P. glaucus in the Black Mountains of North Carolina were mostly yellow. In Tennessee, Kansas, and northern Texas prior to 1884, dark morphs greatly outnumbered the yellow, and in southern Illinois and eastern [TABULAR DATA FOR TABLE 8 OMITTED] Tennessee "yellow females are very rare." Georgia and north-central Florida were reported to have equal numbers of dark and yellow females (Edwards 1884).

The frequencies and distribution limits of dark-morph females appear to have remained surprisingly constant over the last century ([ILLUSTRATION FOR FIGURE 2 OMITTED], Table 2). One conspicuous exception is southern Florida where dark-morph frequencies have increased from less than 10% to nearly 40% since 1960 (Lederhouse and Scriber 1987b). This has been attributed to possible genetic drift associated with habitat loss and drastically reduced population size, but other changes in selection pressures cannot be ruled out.

Genetics of Mimicry in P. glaucus and P. canadensis

The results of this study confirm preliminary evidence of a maternally inherited Y-chromosome dark morph trait (b+) and of an independent inheritable suppression factor in P. canadensis ([s.sup.can]) (see Scriber et al. 1987). The hybrid female offspring (from dark mothers paired with male P. canadensis) are yellow, but this has been shown to be reversible. Dark female offspring can be produced from backcrosses with [TABULAR DATA FOR TABLE 9 OMITTED] males lacking the suppressor (P. glaucus) and in [F.sub.2] crosses. Such reversibility argues against the loss of Y-factor (Clarke and Sheppard 1959, 1962) or an X/Y crossover event, both of which should be too rare to account for our consistent results.

A single X-linked suppressor should yield an equal ratio of dark:yellow female offspring in backcrosses using dark females and hybrid males. In general, there is an excess of dark female offspring (Hagen and Scriber 1989 and Table 9; and also for backcrosses of P. glaucus with P. rutulus; Scriber et al. 1990). Abnormal development of yellow female offspring of dark mothers may reflect incompatibilities of a canadensis X chromosome with glaucus autosomal chromosomes; consistent with Haldane's rule (Haldane 1922, Coyne and Orr 1989, Virdee 1993, Hagen and Scriber 1995).

We have observed exceptions that challenge any simple genetic explanation of color determination (Scriber and Evans 1986; Hagen and Scriber 1989). In addition to the environmentally modulated intermediates caused by high temperatures (Ritland 1986), we have observed some color mosaics with blotches of yellow in an otherwise normal dark-morph female and blotches of dark color in an otherwise normal yellow morph. These aberrations and several perfect and near-perfect bilateral gynandromorphs (half dark and half yellow) probably reflect developmental anomalies (Blanchard and Descimon 1988) and intersexes but may also be related to somatic modification of the expression or suppression of dark color (Scriber and Evans 1988a). We have described other low-frequency polymorphisms and heritable aberrations (Scriber and Lintereur 1983; Scriber and Evans 1988b; Scriber 1990a), which are assumed to be unrelated to the suppressor and dark-morph control.

The second class of abnormalities relates to the nonmaternal-type female offspring colors. Exceptional female offspring (a different color than their mother) occur rarely in frequency in the offspring of field-captured females. We have previously reviewed such cases, including Edward's (1884) report from West Virginia and Clarke and Sheppard's (1959, 1962) reports from Chicago (IL) stock. In view of the discovery of the suppressor phenomenon in P. canadensis (Scriber et al. 1987) and the location of the Chicago stock used by Clarke and Sheppard close to the zone of natural hybrid interaction between the two species in Wisconsin (Scriber 1982; Hagen et al. 1991), it is possible that the odd segregation observed by Clarke and Sheppard (all traceable to the original Chicago source) in the putatively pure P. glaucus was actually from individuals with prior introgression from P. canadensis.

For example, we have observed a low frequency of gene flow across the region between 40 [degrees] N and 45 [degrees] N latitude, which corresponds to the northern limits of the bivoltine potential. This area can be fairly precisely delineated by seasonal thermal unit accumulations (from meteorological data) above the base developmental threshold (10 [degrees] C) for tiger swallowtail caterpillars (Scriber and Lederhouse 1983; Ritland and Scriber 1985; Hagen and Lederhouse 1985). It is evident that the northernmost limits to dark-morph females parallels these thermally defined geographic limits (with some corrections required in the Appalachians because of fine-scale altitudinal effects on thermal accumulations; Scriber and Hainze 1987; Scriber 1988). There is an abrupt decline in frequency of P. glaucus-type allozymes and increase in P. canadensis-type allozymes as one moves northward across central Wisconsin and Michigan (Hagen et al. 1991; Scriber 1994). Our introgression hypothesis could explain the odd segregating wild broods of putative P. glaucus (i.e., dark females) from Wisconsin because these mothers were from Dane County and Green Lake County (Table 3), which are both in the hybrid zone (see also Scriber 1990b). It is even feasible that four odd segregating yellow female offspring from northern Illinois and one from northern Indiana (Table 1) could be accounted for by this hypothesis of P. canadensis gene flow. It is, however, unlikely that such introgression could explain the occurrence of the one yellow female offspring segregant from Florida or the four from Georgia (Table 1).

If females of P. canadensis and the western P. glaucus group species P. eurymedon, P. rutulus, and P. multicaudatus lack the b+ allele for dark color, what then would be the value of a consistently effective suppressor system in these species (Scriber et al. 1990)? In an alternative view, Papilio alexiares garcia (Scriber et al. 1989) and P. glaucus males might have an enabler on the X chromosome that allows dark female offspring expression, instead of the lack of a suppressor. Although our pairings of dark P. glaucus females with the western P. multicaudatus and P. rutulus males resulted in extended female diapause, some females that emerged were intermediate or dark (Scriber et al. 1990). Clarke and Willig (1977) have previously obtained intermediate [F.sub.1] P. glaucus x P. rutulus hybrids by breaking the extended diapause with a-ecdysone injections (see also West and Clark 1988). Thus, the effectiveness of the suppressors varies with the species. If [s.sup.glau] facilitates the expression of b+, then exceptional yellow female offsprong of dark P. glaucus mothers could result from a partially defective [s.sup.glau].

In summary, we still lack a complete understanding of the genetics of color morphs. The single X-linked suppressor/enabler appears the most plausible model. However, linkage with X-chromosome genes influencing viability of hybrids, variation in completeness of dark morph expression (e.g., family #3770), and cases of inheritance patterns that do not follow Mendelian rules, remain to be integrated.

Linkage between Diapause and Color Suppression as an Explanation of the Northernmost Distribution of Dark-Morph P. glaucus Females

The sharp delineation of northern limits to dark females of P. glaucus in Wisconsin and Michigan is virtually identical with the northern limits to bivoltine populations (Scriber et al. 1987; Scriber 1988). Low thermal unit accumulations during the summer result in strong selection against a second generation of tiger swallowtail butterflies north of the Great Lakes hybrid zone even on the very best host plants (Rockey et al. 1987; Scriber and Hainze 1987; Scriber and Lederhouse 1992). Although populations south of the hybrid zone can complete two generations, obligate diapause in the northern half of Wisconsin, Michigan, and north-central New York has been strongly selected for in P. canadensis (Hagen and Lederhouse 1985; Scriber 1994; Scriber and Gage 1995). Control of obligate diapause is sex linked and closely linked with the suppressor locus as well as four allozymes (Acp, Tpi, Pgd, and P3gdh; Hagen and Scriber 1989, 1995).

Strong selection on one of a number of closely linked loci can prevent gene flow of neutral alleles at the others (Barton 1979, 1983; Thompson 1977). A strong selection gradient for obligate diapause may limit northward gene flow from P. glaucus populations with facultative diapause tendencies that are just south of the hybrid zone. The abrupt latitudinal step cline in the frequency of dark-morph females in the Great Lakes region [ILLUSTRATION FOR FIGURE 2 OMITTED] seems just as likely due to these linkage effects as it is due to a parallel selection cline for mimicry of B. philenor (in this northern region the model becomes rare and disappears; Ebner 1970; Opler and Krizek 1984).

In the southeastern United States, the relative abundance of black females is geographically correlated with the abundance of the B. philenor model (Brower 1958; Brower and Brower 1962), which suggests that natural selection for mimetic females may help maintain a color polymorphism. Sexual selection (males preferring yellow females) has been proposed as a factor preventing the Y-linked dark allele from going to fixation (Burns 1966). However, the idea remains unresolved (Pliske 1972; Levin 1973; Platt et al. 1984; Lederhouse and Scriber 1987a; Lederhouse et al. 1989). The dark allele has increased in frequency in southern Florida (Lederhouse and Scriber 1987b and Table 2) despite strong male preference for yellow females (Lederhouse 1995; Lederhouse and Scriber, unpubl. manuscript). Yet, male preference appears to be labile where dark-morph females are abundant.

In the Great Lakes hybrid zone, where the model (B. philenor) becomes rare or absent, there would presumably be reduced selection favoring dark females. We do observe less than 50% dark females about 100 miles south of the hybrid zone and 0-10% dark females within 10-50 miles of the zone. If the frequency of the dark gene (b+) was 0.5 (e.g., St. Joseph County, MI, or Dane County, WI; Table 2) and the suppressor 0.1 in this hybrid zone, then the frequency of exceptional female offspring would be 2bs(1 - s) = 0.09. A lower dark gene frequency (e.g., 0.2) closer to the hybrid zone would yield exceptional genotypes in a frequency of 0.036 (Table 1). Limited introgression between canadensis and glaucus as indicated by multivariate morphometric techniques (Luebke et al. 1988), and the actual frequencies observed near the hybrid zone [ILLUSTRATION FOR FIGURE 2 OMITTED] suggest that this simple model may be realistic. The odd segregating female offspring generally represent less than 5% of the totals.

Even weak parallel clines in other selection pressures (such as diapause regulation or thermal adaptation; Feder and Bush 1989), however, could act simultaneously upon this Great Lakes hybrid zone to keep it quite narrow, especially for sex-linked loci (Barton 1983, Orr 1993), despite the potential for considerable dispersal of adults (Lederhouse 1982). We are currently investigating various biotic and abiotic factors affecting gene flow (including b and s) within and across this hybrid zone for P. glaucus and P. canadensis.

ACKNOWLEDGMENTS

This research was supported in part by the College of Agriculture and Natural Resources (MAES Project #8051, 1644, and 8072) and the College of Natural Science at Michigan State University and by the National Science Foundation (BSR 87 18448, BSR 90 01391, BSR 91 07139, and DEB 92 20122), United States Department of Agriculture grants (#87-CRCR-1-2851 and 90-37153-5263), and in part by the NSF-sponsored LTER at Kellogg Biological Station. We would particularly like to thank the following people for valuable discussion and/or their assistance in field collections for this study or for use of their personal and institutional research collections: T Allen, Y. Allen, M. Ayres, D. Baggett, P. Barker, M. Berenbaum, W. Bergman, D. Biddinger, S. Borkin, J. Bossart, D. Brockway, R. Brown, C. Bryson, J. Calhoun, C. Codella, M. Collins, C. Clarke, R. Dowell, G. Drecktrah, M. Evans, L. Ferge, I. Finkelstein, R. Fisher, B. Giebink, G. Godfrey, W. Gould, E. Grabstein, D. Grossmueller, K. Hale, S. Heg, T. Herrig, W. Houtz, D. Iftner, J. Johnson, K. Johnson, R. Kergosian, K. C. Kim, P. Kingsley, R. Lindroth, G. Lintereur, H. Luebke, S. Manuwoto, B. Mather, D. Matusik, J. Maudsley, S. Maclean, J. Miller, L. Miller, B. Mohr, M. Neilsen, J. Nitao, A. Norrbon, H. Pavulaan, R. Piegler, S. Peterson, T. Pike, J. Pomraning, C. Plzak, D. Ritland, J. Schrimpft, R. Schaefer, T. Schiefer, A. Shapiro, E. Schuh, J. Shuey, J. Siebenhorn, K. Simpson, C. Smith, D. Snider, B. Taft, J. Thompson, J. Thorne, B. Warfield, T. Uhlman, V. Viegut, W. Wehling, D. West, and A. Young.

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Author:Scriber, J. Mark; Hagen, Robert H.; Lederhouse, Robert C.
Publication:Evolution
Date:Feb 1, 1996
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