Variation in wing pattern and palatability in a female‐limited polymorphic mimicry system

Checkerspot butterflies in the genera Euphydryas and Chlosyne exhibit phenotypic polymorphisms along a well‐defined latitudinal and elevational gradient in California. The patterns of phenotypic variation in Euphydryas chalcedona, Chlosyne palla, and Chlosyne hoffmanni suggest a mimetic relationship; in addition, the specific patterns of variation in C. palla suggest a female‐limited polymorphic mimicry system (FPM). However, the existence of polymorphic models runs counter to predictions of mimicry theory. Palatability trials were undertaken to assess whether or not the different color morphs of each species were distasteful or toxic to a generalized avian predator, the European starling (Sturnus vulgaris). Results indicate that the black morph of E. chalcedona is distasteful, but not toxic, to predators, while the red morph is palatable. C. hoffmanni and both color morphs of C. palla are palatable to predators. Predators that learn to reject black E. chalcedona also reject black C. palla, suggesting that the latter is a FPM of the former. C. hoffmanni does not appear to be involved in this mimetic relationship.     

The ecology and population genetics of an alpine checkerspot butterfly,Euphydryas anicia

Summary The population structure, ecology and genetics of alpine and subalpine populations of Euphydryas anicia were investigated in Gunnison County, Colorado. Distances moved by individuals between recapture events at Cumberland Pass, elevation 3700 m, averaged less than 100 meters, but were greater than for most Euphydryas populations and other alpine Euphydryas populations in particular. Individuals often moved long distances, in patterns reminiscent of Euphydryas chalcedona populations and the more vagile populations of E. editha. The population size of 50,000 to 100,000 individuals was the largest encountered in nineteen years of studying dozens of Euphydryas populations. Gene frequencies at nine allozyme loci were determined for the population in 1974 through 1977, and in other Colorado E. anicia populations in several of those years. Although large population sizes make drift unlikely, genetic differences were detected between samples taken in different years. Genetic differences were also detected between this and other alpine E. anicia populations, although there is some indication that E. anicia shows less genetic differentiation than E. editha or E. chalcedona.     

Population biology of the checkerspot butterfly,Euphydryas chalcedona structure of the Jasper Ridge colony

Summary Euphydryas chalcedona at Jasper Ridge consists of two independently varying major demographic units, similar in scale but not in structure to those of Euphydryas editha. In contrast, however, Jasper Ridge E. chalcedona represent just a portion of a deme-while E. editha occurs as two partially connected demes. The life history and general ecology of E. chalcedona is described and compared with those of its intensively-studied congener. Various problems of mark-release-recapture estimation of population size are discussed     

Ecological determinants of food plant choice in the checkerspot butterfly Euphydryas editha in Colorado

Summary The larvae of Euphydryas editha in Gunnison County, Colorado, feed on Castilleja linariifolia. Two related plants, C. chromosa and Penstemon strictus, occur in the same area and are equally nutritious, but are not eaten. Restriction to C. linariifolia appears to be a case of ecological monophagy — survival on the other two species is less likely not because of their biochemical make-up but because of their ecological characteristics, primarily their phenologies.     

Host‐associated genomic differentiation in congeneric butterflies: now you see it,now you do not

Ecotypic variation among populations may become associated with widespread genomic differentiation, but theory predicts that this should happen only under particular conditions of gene flow, selection and population size. In closely related species, we might expect the strength of host‐associated genomic differentiation (HAD) to be correlated with the degree of phenotypic differentiation in host‐adaptive traits. Using microsatellite and Amplified Fragment Length Polymorphism (AFLP) markers, and controlling for isolation by distance between populations, we sought HAD in two congeneric species of butterflies with different degrees of host plant specialization. Prior work on Euphydryas editha had shown strong interpopulation differentiation in host‐adapted traits, resulting in incipient reproductive isolation among host‐associated ecotypes. We show here that Euphydryas aurinia had much weaker host‐associated phenotypic differentiation. Contrary to our expectations, we detected HAD in Euphydryas aurinia, but not in E. editha. Even within an E. aurinia population that fed on both hosts, we found weak but significant sympatric HAD that persisted in samples taken 9 years apart. The finding of significantly stronger HAD in the system with less phenotypic differentiation may seem paradoxical. Our findings can be explained by multiple factors, ranging from differences in dispersal or effective population size, to spatial variation in genomic or phenotypic traits and to structure induced by past histories of host‐adapted populations. Other infrequently measured factors, such as differences in recombination rates, may also play a role. Our result adds to recent work as a further caution against assumptions of simple relationships between genomic and adaptive phenotypic differentiation.     

Protandry and postandry in two related butterflies: conflicting evidence about sex-specific trade-offs between adult size and emergence time

Natural selection acting on timing of metamorphosis can be sex-specific, resulting in differences in timing between males and females. Insects with discrete generations frequently show protandry: males usually mature before females. Both Euphydryas editha and E. aurinia butterflies followed this trend. The present study was motivated by the unusual observation of consistent postandry in addition to protandry. In a single E. editha population observed over 20 years the emergence period of males was longer than that of females, both the first and last emerging individuals being males. Variance of timing among individual E. editha larvae is imposed by spatial patchiness of the snowmelt that releases them from winter diapause. If individual larvae released late from diapause were to compensate for their lateness by shortening their development times, they would be small at maturity. If such compensation were only partial, they would be both late and small. Size and timing would become associated. If females were more prone to such partial compensation than males, the observations of postandry could be explained and the prediction made that any tendency for late individuals to be small should be stronger in females than in males. This was the case: in 1 year late males were the same size as early males, in a second year they were larger. Late females were significantly smaller than early females in both years. In E. aurinia, results were opposite both to theoretical prediction and to the observations from E. editha: although the male emergence period was longer than that of females exactly as in E. editha, late males were smaller than early ones, while late females were not small. The data from E. editha support the hypothesis of a sex-specific trade-off between size and emergence time, the data from E. aurinia do not.     

INCORPORATION OF A EUROPEAN WEED INTO THE DIET OF A NORTH AMERICAN HERBIVORE

Populations of the butterfly Euphydryas editha living within a 30 times 100–km region on the eastern slope of the Sierra Nevada range were compared for oviposition preference and ability of larvae to grow and survive on two host plants, Collinsia parviflora and Plantago lanceolata. Since its introduction approximately 100 years ago, P. lanceolata has been incorporated in the diet of E. editha in one of the study populations. The populations differed in oviposition preference; only the population that uses P. lanceolata contains some individuals that prefer P. lanceolata. Larvae from two populations, one using both P. lanceolata and C. parviflora, the other using only C. parviflora, were not found to differ in relative abilities to grow or survive on P. lanceolata. The potential for E. editha to use P. lanceolata appears in populations that have had no prior exposure to this plant, while oviposition preference for this plant has evolved in the population in which the plant now grows.     

Rainfall and the interaction of microclimate with larval resources in the population dynamics of checkerspot butterflies (Euphydryas editha) inhabiting serpentine grassland

Summary The interaction of host plant phenology and microclimatic heterogeneity was examined to determine its role in the population dynamics of checkerspot butterflies, Euphydryas editha, inhabiting serpentine grassland in California's outer Coast Range.Within the 2–3 hectares inhabited by a population of E. editha (Jasper Ridge Area H), microclimatic differences resulting from topographic heterogeneity largely determine the temporal and spatial pattern of senescence of the larval host plants, Plantago erecta and Orthocarpus densiflorus. Survival of larvae from hatching to diapause is extremely low as a result of unpredictable variation in the timing of larval development relative to the timing of host plant senescence, both of which are mediated by microclimatic patterns. During this study, population H declined to near extinction as a result of two consecutive years of record rainfall that apparently disrupted the tenuous temporal relationship between larval development and plant senescence. Retarded development of post-diapause larvae led to a late and extended flight season and delayed egg production; this in turn resulted in massive mortality of pre-diapause larvae due to starvation because host plant senescence occurred before larvae became large enough to enter diapause. Adult population size the following spring was the smallest in 25 years of study. This work emphasizes the importance of microclimatic heterogeneity for understanding population-level processes in small ectothermic animals and underlines the potential importance of such heterogeneity in the establishment of reserves designed to protect such animals     

Diet divergence in two sympatric congeneric butterflies: Community or species level phenomenon?

Summary Two species ofEuphydryas butterflies were studied in California, USA, and showed considerable diet overlap at the species level. They utilize many of the same plant genera for oviposition. However,E. editha is less likely to use woody perennials than isE. chalcedona.Both butterfly species are known to specialize on different host plants in different populations, so species level divergence may not be a good predictor of community level divergence. Within five communities,E. editha andE. chalcedona showed no dietary overlap. A major component of the niche ofE. editha in one community was occupied byE. chalcedona in a second community, even though both butterfly species occupied both communities. These resource use patterns indicate that community level interactions may affect diet divergence. The degree to which divergence within communities is greater (or less) than expected from a species level comparison may be used to provide a measure of community organization. Equations are given in the Appendix for calculating overlap probabilities from presence/absence types of data; in this study, presence is oviposition on a particular plant species, absence is no oviposition on that plant species. Given the various assumptions of the model,E. editha andE. chalcedona show significant community level components of their dietary divergence in the areas studied. However, in some other communitiesE. editha andE. chalcedona do share host plant species. Therefore, we could not demonstrate community level divergence conclusively, nor has this been demonstrated for any other pair of insect herbivore species. We do not know whether this is because the phenomenon is truly rare or just very hard to demonstrate.     

Quantification of host preference by manipulation of oviposition behavior in the butterfly Euphydryas editha

Summary This paper describes a novel method of measuring host specificity and determining host rank order. As applied to oviposition behavior of the butterfly Euphydryas editha, the rank order of preference is the order in which plants become acceptable as the insect searches, while specificity is quantified in terms of the rate at which searching insects become less discriminating. The information obtained is different from that gleaned from other preference testing techniques. It is useful in helping to assess the behavioral bases of interpopulation differences in the degree of host specialization, in understanding the ways in which multiple host use is generated within a population, and in testing hypotheses about the evolution of host specialization.The data presented here show interpopulation variation in both rank order of host species and in the degree of host specificity of E. editha.     

Pre- and post-alighting host discrimination by Euphydryas editha butterflies: The behavioural mechanisms causing clumped distributions of egg clusters

Egg clusters of the checkerspot butterfly, Euphydryas editha, are contagiously distributed among host plants (Pedicularis semibarbata) at one mid-elevation montaine site in California. Large, isolated plants receive more egg clusters than is expected from their proportional representation in the population. This study attempts to determine the behavioural causes of that contagious distribution.Non-random alighting by ovipositing females appears to be the primary cause of the observed contagious distribution. Females alight more often than would be expected by chance on large, isolated plants. Females also appear to exhibit a weak post-alighting bias in favour of large, isolated plants, though this bias is not statistically significant. However, manipulative experiments reveal that postalighting acceptance is not random; certain plants are accepted repeatedly while others are rejected repeatedly. The results also indicate that searching females distinguish among different classes of plants within a host species.     

Conspecific host discrimination by ovipositingEuphydryas editha butterflies: Its nature and its consequences for offspring survivorship

Ovipositing E. editha butterflies display post-alighting discrimination among patches of Collinsia torreyi, one of their major hosts in the General's Highway (GH) population at a montane site in California. Females tended to accept (i.e. oviposit on) dense patches of this host and to reject sparse patches. Possible behavioural mechanisms underlying this tendency are discussed. The consequences of this non-random pattern of oviposition for egg and larval survivorship were investigated and no differences were found in the survivorship of larvae on acceptable and unacceptable collinsias.     

Mimicry in North American checkerspot butterflies: Euphydryas phaeton and Chlosyne harrisii (Nymphalidae)

ABSTRACT.

• 1 An examination of the phenetics, ecology and distribution of Chlosyne harrisii suggested that it was a potential mimic of the unpalatable Euphydryas phaeton.
• 2 The wing undersurfaces of the adults are very similar and the larvae are virtually identical. The geographic range of both butterflies is the northeastern United States and both are inhabitants of wet meadow habitats where they may fly together. The life histories of both species are closely synchronized.
• 3 A series of feeding experiments using blue-jays as predators showed first, that C.harrisii is palatable, and second, suggested that the birds could not distinguish between C.harrisii and E.phaeton on the basis of visual cues. Thus, Charrisii seems to be an effective Batesian mimic of E.phaeton.

     

Butterfly larvae reduce host plant survival in vicinity of alternative host species

Summary Mortality of an annual plant. Collinsia torreyi, was increased in the vicinity of Pedicularis semibarbata plants. This was a consequence of feeding by Euphydryas editha, a herbivore which feeds on both plant species. Mortality of C. torreyi was better predicted by distance from P. semibarbata than by density of C. torreyi. Since not all herbivores are monophagous, interactions involving distance and density effects on plant survival and on vegetational diversity need to be considered with respect to plant and herbivore communities. Some of the complexities of one predator, two prey systems are discussed.     

REPEATED REVERSALS OF HOST-PREFERENCE EVOLUTION IN A SPECIALIST INSECT HERBIVORE

A tree of mitochondrial DNA (mtDNA) haplotypes was constructed to estimate the number of evolutionary changes of host-plant preference needed to account for variation among 24 populations of the butterfly Euphydryas editha. Using 17 restriction endonucleases, 22 mtDNA haplotypes were found among 24 populations of this butterfly species. We allowed for the possibility of haplotypes to acquire particular preferences either from evolutionary change at their local sites or from migration to populations where those preferences occurred. After we had taken these estimates of migration into account, a minimum of 10 evolutionary changes of host preference (reduced from 22) was needed to explain the pattern of use of five host-plant genera among these populations. Analysis of allozyme variation among a partially overlapping set of populations also suggested multiple host shifts. Although genetic variation of host preference is largely responsible for interpopulation variation of diet, repeated reversals of preference evolution have occurred. However, host preferences were not distributed randomly with respect to phylogeny, and some tendency toward evolutionary conservation of preference also was indicated. The haplotype of E. editha most closely related to the sister species, E. chalcedona, used a principal host of E. chalcedona. Our results suggest that host shifts occur frequently in E. editha, are a result of both migration and local evolution, and have not been associated with speciation in these insects.     

Long range dispersal in checkerspot butterflies: Transplant experiments with Euphydryas gillettii

Summary Transfers of eggs and larvae from montane Wyoming populations of Euphydryas gillettii south to locations in the central Colorado mountains have resulted in the establishment of at least one Colorado population. This result shows that the previous absence of the species from Colorado was the result of its inability to cross the barrier of the Wyoming Basin, not the ecological unsuitability of Colorado habitats. This, in turn, supports the contention that Euphydryas do not easily disperse long distances.Dedicated to Dr. Konrad F. Springer     

Effect of cultivating croplands and grazing in arid grassland habitats on the conservation of melitaeine butterflies in a mountainous area in Northern China

In the study area (Yanjiaping Village, Hebei Province, China), grazing extensity varies at different locations, small and discontinuous croplands are imbedded in some arid grassland, which are habitats for the melitaeine butterflies, Euphydryas aurinia and Melitaea phoebe. These two species of butterfilies coexist in this area, in which grazing and cultivation are the main disturbances. Grazing and cultivation have a reciprocal effect on E. aurinia, rather than M. phoebe. We observed that E. aurinia preferred to occupy patches with moderate grazing and imbedded with small and discontinuous croplands, where E. aurinia also has high population density. The percentage of E. aurinia larval groups in the ribbings was significantly higher than that of M. phoebe, whereas larvae of both species tended to increase in recent years. Our data also showed that the population density and the patch occupancy rate of both E. aurinia and M. phoebe were the highest under moderate grazing. It indicates that cultivation of small and discontinuous croplands within the patch has a significant effect on the population density of both species of melitaeine butterflies. Thus, to artificially create or maintain semi-natural habitats, complemented by moderate grazing, might be an ecological strategy to conserve melitaeine butterflies effectively. Considering the distinct impacts of cultivation and grazing on the population distribution and dynamics of the two different species, human disturbance in the mountainous area might be strategically involved in proposing conservation plans for the target species in the future.     

Variation among individual butterflies along a generalist–specialist axis: no support for the 'neural constraint' hypothesis

Abstract 1. Degree of host specialisation was a continuous variable in a population of Edith’s checkerspot butterfly (Euphydryas editha). A novel host, Collinsia torreyi, had been added to the diet in response to anthropogenic disturbance, and then abandoned prior to the current study. Butterflies either showed no preference or preferred their traditional host, Pedicularis semibarbata. 2. Strength of preference for Pedicularis over Collinsia was measured in the field and used to estimate host specialisation of individual butterflies. Efficiency was estimated from the times taken by each insect to perform two tasks: (i) identification of a Pedicularis plant as a host, and (ii) successful initiation of oviposition after the decision to do so had been made. 3. There was no clear trend for association between host specialisation and either measure of efficiency. Generalists were not slower than specialists at identifying Pedicularis as a host or at handling it after deciding to oviposit. 4. Prior work indicated that generalists paid no detectable cost in terms of reduced discrimination among individuals of their preferred host species. 5. In contrast to other species, generalist E. editha paid in neither time nor accuracy. Why then does the diet not expand? Behavioural adaptations to the traditional host caused maladaptations to the novel host and generated short‐term constraints to evolutionary expansion of diet breadth. To date, however, no long‐term constraints have been found in this system. In those traits investigated to date, increased adaptation to the novel host has not caused reduced adaptation to the traditional host.     

The role of adult feeding in egg production and population dynamics of the checkerspot butterfly Euphydryas editha

Carbohydrate intake increases longevity, body weight maintenance and egg production in female Euphydryas editha. Amino acid intake leads to heavier eggs, larvae from which are more likely to survive. Females fed nectar produce more eggs in later masses than females which are not fed. During years of normal and below normal precipitation, larvae emerging from these later eggs are unlikely to reach obligatory size for diapause before their food dries up. On Jasper Ridge, where mortality is density-independent, nectar plays an important role increasing production of late egg masses during years of greater than normal rainfall when larvae from these masses are likely to reach diapause. The resulting large population increases, though infrequent, are probably important in maintaining population sizes large enough to reduce the chances of extinction during dry years.     

Population genetic structure of the round stingray Urobatis halleri (Elasmobranchii: Rajiformes) in southern California and the Gulf of California

The round stingray, Urobatis halleri, is a viviparous elasmobranch that inhabits inshore, benthic habitats ranging from the western U.S.A. to Panama. The population genetic structure of this species was inferred with seven polymorphic microsatellite loci in samples collected at three sites in coastal southern California, one near Santa Catalina Island, California and one in the eastern Gulf of California. Urobatis halleri is relatively common, but little is known of its movement patterns or population structure. Small F_ST values (?0·0017 to 0·0005) suggested little structure among coastal populations of southern and Baja California. The population sampled at Santa Catalina Island, which is separated by a deep‐water channel from the coastal sites, however, was significantly divergent (large F_ST, 0·0251) from the other populations, suggesting low connectivity with coastal populations. The Santa Catalina Island population also had the lowest allele richness and lowest average heterozygosity, suggesting recent population bottlenecks in size.