Michael C. Singer

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.

The Definition and Measurement of Oviposition Preference in Plant-Feeding Insects

For many plant-feeding insects, the selection of an ovipositon site is a critical stage in their choice of host. This is especially true when the newly hatched offspring are not capable of searching for additional hosts until they have fed on the individual chosen by their mother (but see Wint, 1983; Futuyma et al., 1984). An understanding of the physiological, behavioral, ecological, or evolutionary interactions between these insects and their hosts requires precise representation of the events and factors influencing oviposition. Ecologists and entomologists have tried to simplify the complex processes involved by using shorthand terms to represent abstract concepts that summerize the most pertinent variables. For example, insect preference and host acceptability summarize the array of factors determining the immediate outcome of a particular encounter between insect and plant, whereas larval performance, host suitability, and plant response to attack describe the subsequent consequences of oviposition. These and other concepts have been used in a variety of ways by different authors, many of whom have failed to define and distinguish among the terms they have used.

EVOLUTION OF FOOD-PLANT PREFERENCE IN THE BUTTERFLY EUPHYDRYAS EDITHA

A ten-year study of the biology of the Jasper Ridge colony of the nymphaline butterfly Eupkydryas editka has combined yearly estimation of population size and structure with phenetic studies (Ehrlich, 1965; Mason, Ehrlich, and Emmel, 1967; Ehrlich and Mason, 1966). The results obtained have been clarified by behavioral (Labine, 1967), ecological (Singer, unpub.) and genetic (McReynolds, ms.: Singer and Gilbert, ms.) studies through the whole life cycle of the insect at Jasper Ridge. This work has now been expanded into a broad ecological comparison of numerous populations living in different types of community, stressing the relationships between E. editka and other organisms such as food plants, nectar sources and predators. As part of this comparison, interpopulation differences in oviposition preference have been investigated in two ways; by laboratory testing and by direct observation in the field. Where evidence as to proximate mechanisms responsible for these differences can be obtained, this can be regarded as evidence of the mechanisms involved in microevolutionary changes of oviposition preference in E. editha. Such changes in oligophagous insects are usually assumed to be changes in chemotactic response; the literature on insect food-plant preferences, reviewed by Thorsteinson (1960), stresses such chemotactic responses. This paper presents evidence that microevolutionary changes in oviposition preference may occur by means others than changes in chemotaxis. It should be noted that larval food-plant preference is not related to adult oviposition preference in any predictable way, and will be the subject of a subsequent paper in this series. The

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

SummaryThis 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.

Phenological asynchrony between herbivorous insects and their hosts: signal of climate change or pre-existing adaptive strategy?

Climate change alters phenological relations between interacting species. We might expect the historical baseline, or starting-point, for such effects to be precise synchrony between the season at which a consumer most requires food and the time when its resources are most available. We synthesize evidence that synchrony was not the historical condition in two insect–plant interactions involving Ediths checkerspot butterfly (Euphydryas editha), the winter moth (Operophtera brumata) and their host plants. Initial observations of phenological mismatch in both systems were made prior to the onset of anthropogenically driven climate change. Neither species can detect the phenology of its host plants with precision. In both species, evolution of life history has involved compromise between maximizing fecundity and minimizing mortality, with the outcome being superficially maladaptive strategies in which many, or even most, individuals die of starvation through poor synchrony with their host plants. Where phenological asynchrony or mismatch with resources forms the starting point for effects of anthropogenic global warming, consumers are particularly vulnerable to impacts that exacerbate the mismatch. This vulnerability likely contributed to extinction of a well-studied metapopulation of Ediths checkerspot, and to the skewed geographical pattern of population extinctions underlying a northward and upward range shift in this species.

Extinction, Reduction, Stability and Increase: The Responses of Checkerspot Butterfly (Euphydryas) Populations to the California Drought

SummaryThe California drought of 1975–77 has been correlated with unusual size changes in populations of two species of Euphydryas butterflies. Several populations became extinct, some were dramatically reduced, others remained stable and at least one increased. These differences in population dynamic response are not concordant with predictions made earlier that populations with heavy density-dependent mortality should be more stable in the face of drought than unregulated populations. The different responses are related to the fine details of the relationships between the insects and their host plants, relationships which are variable between populations. Revised predictions are given in the light of better knowledge of the variability and complexity of these insect-host relationships. The diversity of responses underlines the dangers of generalizing about “the ecology” of a taxonomic species. The extinctions support the view that such events are frequent and significant in the biology of populations.

Complex Components of Habitat Suitability within a Butterfly Colony

The microdistribution of adult Euphydryas editha changes from year to year, and the colony is subdivided into three populations that fluctuate independently in size. These observations are attributed largely to fluctuations in time and space of three complex larval resources associated with the availability of food. This cotnplexity also entails selection pressure favoring the observed low dispersal tendency of adults.

Experimental confirmation that inbreeding depression increases extinction risk in butterfly populations.

1. Department of Ecology and Systematics, Division of Population Biology, P.O. Box 17 (Arkadiankatu 7), University of Helsinki, FIN-00014 Helsinki, Finland; 2. Section of Integrative Biology, University of Texas, Austin, Texas 78712; 3. Sydväst Polytechnic, Forstinstitutsvägen, FIN-10600 Ekenäs, Finland; 4. Lehrstuhl für Landschaftsökologie, Christian-Albrechts-Universität, Hermann-Rodewaldstr. 9, D-24098 Kiel, Germany

Catastrophic Extinction of Population Sources in a Butterfly Metapopulation

Increasing emphasis is being placed on the large-scale and long-term dynamics of populations. A butterfly (Euphydryas editha) metapopulation that was naturally restricted to rocky outcrops in an area of coniferous forest suffered two major perturbations in 30 yr. First, humans clear-cut patches of forest in about 1967. The butterfly colonized the clear-cuts, in which it began to oviposit on a novel host plant, Collinsia torreyi. Breeding success was high, and the clear-cut habitat supported a population source; in the mid-1980s, there was net movement of adults from clear-cut to outcrop, and butterfly densities were elevated on outcrops close to population sources. The second major perturbation came in 1992, when a severe summer frost killed C. torreyi plants (outcrop hosts were not damaged). As a result, E. editha larvae starved in clear-cuts, and the source populations became extinct. This occurrence allowed us to test several predictions of source-sink theory. As predicted, densities declined on outcrops, and particularly on those close to former sources; by 1993, densities on outcrops were no longer correlated with isolation from former sources. True population sinks are predicted to become extinct in the absence of immigration, but this prediction was not observed. Outcrops were not true sinks because E. editha occupied this habitat before the creation of sources, survived the frost on outcrops, and persisted on outcrops in areas where they were isolated from sources. Outcrops were pseudosinks; breeding success was poor at immigration-enhanced densities, but outcrop populations did not rely on immigration to persist. The implications for conservation biology are that populations with high mean density and that act as sources are not necessarily more stable than lower-density or pseudosink populations. This may be especially true of systems subject to recent human disturbance, as in the present case.

Extinction‐Colonization Dynamics and Host‐Plant Choice in Butterfly Metapopulations

Species living in highly fragmented landscapes often occur as metapopulations with frequent population turnover. Turnover rate is known to depend on ecological factors, such as population size and connectivity, but it may also be influenced by the phenotypic and genotypic composition of populations. The Glanville fritillary butterfly (Melitaea cinxia) in Finland uses two host‐plant species that vary in their relative abundances among distinct habitat patches (dry meadows) in a large network of ∼1,700 patches. We found no effect of host species use on local extinction. In contrast, population establishment was strongly influenced by the match between the host species composition of an empty habitat patch and the relative host use by larvae in previous years in the habitat patches that were well connected to the target patch. This “colonization effect” could be due to spatially variable plant acceptability or resistance or to spatially variable insect oviposition preference or larval performance. We show that spatial variation in adult oviposition preference occurs at the relevant spatial scale and that the other possible causes of the colonization effect can be discounted. We conclude that the colonization effect is generated by host preference influencing the movement patterns of ovipositing females. Migrant females with dissimilar host preferences have different perceptions of relative patch quality, which influences their likelihood of colonizing patches with particular host composition.