The structure and genetics of a montane population of the checkerspot butterfly,Chlosyne palla

Summary The population structure, genetics and ecology of the checkerspot butterfly, Chlosyne palla, in an area of Gunnison County, Colorado were investigated. The population structure was found to be quite different from that of most butterflies and from all of those aspects known for its thoroughly studied relative, Euphydryas editha. The population unit of Chlosyne palla may cover an area some five to eight times the size of the largest known Euphydryas population and twice the size of an Erebia epipsodea population in the same county of Colorado.Genetic variation at eleven loci of Chlosyne palla was examined by electrophoresis. Three samples of Chlosyne palla separated by 1.6, 4.7, and 12.0 km were not significantly different. Comparison with Euphydryas editha yields a genetic similarity of 0.186, about the same level as found by Ayala (1975) for different genera of Drosophila. Euphydryas editha from the same Colorado location were more similar to California E. editha than to C. palla, showing concordance with the phenetic classification. Decreased heterozygosity was observed for the Colorado E. editha and C. palla compared to California populations of E. editha and E. chalcedona.     

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.     

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.     

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     

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.     

Nectar source distribution as a determinant of oviposition host species in Euphydryas chalcedona

The distribution of nectar sources is shown to affect both the distribution of adult Euphydryas chalcedona and their offspring. We suggest that nectar sources thereby influence the selection of oviposition host plant species in habitats where those species are spacially separated.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

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 coevolution of Euphydryas chalcedona butterflies and their larval host plants

Summary The interactions between the checkerspot butterfly, Euphydryas chalcedona, and two of its principal host plants, Diplacus aurantiacus and Scrophularia californica, were studied to test the hypothesis that feeding behavior in nature reflects food quality in terms of leaf nitrogen and defensive chemical contents. Larvae preferentially fed on Diplacus leaves containing the highest nitrogen: resin ratio in the field and laboratory. Larvae did not feed selectively among Scrophularia leaves, which show little variation in quality. Seasonal timing of feeding activity and larval development rates were closely related to the availability of any Scrophularia leaves and high-quality Diplacus leaves.     

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.     

MULTITRAIT,HOST‐ASSOCIATED DIVERGENCE AMONG SETS OF BUTTERFLY POPULATIONS: IMPLICATIONS FOR REPRODUCTIVE ISOLATION AND ECOLOGICAL SPECIATION

When populations use different resources, they tend to diverge in traits that affect performance on those resources. The extent and complexity of divergence that is achieved will depend on gene flow, genetic constraints, and the character of divergent selection. We describe divergent host adaptation among Californian populations of the Melitaeine butterfly, Euphydryas editha. Divergence in seven traits created parallel phenotypic suites, each suite associated with the use of a different host species, either Collinsia torreyi or Pedicularis semibarbata. The suites involved alighting responses of adults (probably to visual stimuli), chemosensory responses to leaf surfaces, vertical positioning of adults and larvae (probably due to geotaxis), partitioning of reproductive effort among clutches, and larval performance. Remarkably, the divergent suites did not occur sympatrically, despite ubiquitous co‐occurrence of the hosts, and we know of only one site where any Collinsia species is used sympatrically with another host. In contrast, E. editha often uses two host genera sympatrically when neither of them is Collinsia. We suggest that adaptation to Collinsia is incompatible with adaptation to other hosts and may generate extrinsic postzygotic reproductive isolation among populations. Despite the apparent rarity of host‐shift‐associated speciation in Melitaeine butterflies, adoption of Collinsia as a host may lead to allopatric ecological speciation.     

Herbivory on Diplacus aurantiacus shrubs in sun and shade

This study tested the hypothesis that carbon allocation to the production of leaf antiherbivore chemicals reflects the intensity of herbivory and interacts with resource allocation to photosynthesis. The amount of herbivory by Euphydryas chalcedona butterfly larvae was measured on Diplacus aurantiacus shrubs growing in different daily solar irradiance regimes. The amount of herbivory sustained by plants was directly related to the degree of solar irradiance the shrubs received and to characteristics which vary with light intensity, e.g. leaf specific weight, but not to leaf resin or nitrogen content. Carbon allocation to the defense of leaf area was marginally related to the light regime, but was not directly related to photosynthetic income.     

Native and Non‐Native Community Assembly through Edaphic Manipulation: Implications for Habitat Creation and Restoration

Chemical and physical (abiotic) conditions can be determining factors of community assembly and invasibility, but can this observation be used as a practical tool for habitat creation? Serpentine soils, in particular, have three abiotic components thought to confer invasion resistance: a low Ca:Mg ratio, low water‐retention capacity, and high concentrations of heavy metals. Consequently, not only do some serpentine‐adapted native plants persist only on serpentine soils, but also the community members that depend upon those plants become dependent upon serpentine as well. In an effort to provide additional habitat for the threatened and serpentine‐restricted Bay checkerspot butterfly (Euphydryas editha bayensis), we experimentally altered a non‐serpentine site to mimic the abiotic conditions of serpentine. Attempts to lower the Ca:Mg ratio of soils through the addition of MgSO₄ were unsuccessful. We then altered soil depth through the addition of gravel beds to determine the effects of water stress on native and non‐native community composition. We found that shallow soils had lower water content and correspondingly had significantly lower non‐native species richness and cover. The results present promising means, but also cautionary information, for habitat creation efforts and demonstrate the possible utility of edaphic manipulation in abating non‐native plant invasions. None of the experimental plots supported communities capable of sustaining E. editha populations, emphasizing that the manipulation of physical conditions is only likely to be successful in coordination with other restoration techniques.     

HERITABILITY OF OVIPOSITION PREFERENCE AND ITS RELATIONSHIP TO OFFSPRING PERFORMANCE WITHIN A SINGLE INSECT POPULATION

Within a population of the butterfly Euphydryas editha that oviposits predominantly on two host species, heritable variation in postalighting oviposition preference was found. In a separate experiment, oviposition preference of adult females was found to be correlated with offspring performance (growth). There was a significant tendency for offspring to perform better on the host species that their female parent preferred. Analysis of the data showed that no single factor, neither maternal preference nor the host species on which the offspring were raised, accounted for any significant variation in larval performance. However, the effect of the interaction between host species and maternal preference on offspring performance was highly significant. These findings imply specialization in both oviposition preference and offspring performance by individuals within a single population. With present evidence, this preference-performance correlation is likely to be genetic. However, as in previous studies, other interpretations cannot be excluded.