The and Evolution of Melitaeine

Niklas Wahlberg

Metapopulation Research Group Department of Ecology and Systematics Division of Population Biology University of Helsinki

Academic dissertation

To be presented, with permission of the Faculty of Science of the University of Helsinki, for public criticism in the lecture room of the Department of Ecology and Systematics, P. Rautatiekatu 13, on October 27, 2000, at 12 o’clock noon.

Helsinki 2000 © Niklas Wahlberg, pp. 7–26

Technical editing by Johan Ulfvens

Author’s address: Metapopulation Research Group Department of Ecology and Systematics Division of Population Biology P.O. Box 17 (Arkadiankatu 7) 00014 University of Helsinki Finland e-mail: [email protected]

ISBN 952-91-2615-8 (nid) ISBN 952-91-2688-3 (pdf) Oy Edita Ab Helsinki 2000 Helsinki 2000 The Ecology and Evolution of Melitaeine Butterflies

Niklas Wahlberg

Metapopulation Research Group Department of Ecology and Systematics Division of Population Biology P.O. Box 17 (Arkadiankatu 7) 00014 University of Helsinki Finland

The thesis is based on the following articles:

I Wahlberg, N. & Zimmermann, M. 2000. Pattern of phylogenetic relationships among members of the (: ) inferred from mtDNA sequences. – Cladistics 16, in press.

II Wahlberg, N. 2000. The phylogenetics and biochemistry of host specialization in melitaeine butterflies (Lepidoptera: Nymphalidae). – Submitted manuscript.

III Wahlberg, N., Klemetti, T., Selonen, V. & Hanski, I. 2000. Metapopulation structure and movements in five of checkerspot butterflies. – Manuscript.

IV Wahlberg, N., Moilanen, A. & Hanski, I. 1996. Predicting the occurrence of in fragmented landscapes. – Science 273: 1536-1538.

V Wahlberg, N., Klemetti, T. & Hanski, I. 2000. Dynamic populations in a dynamic landscape: the metapopulation structure of the . – Manuscript.

These are referred to by their Roman numerals in the text. 4 Contributions

Contributions

The following table shows the major contributions of authors to the original articles.

I II III IV V

Original idea NW, MZ NW IH, NW IH TK, IH, NW Study design NW NW NW IH, NW TK, NW Methods and implementation NW NW NW IH, AM, NW NW, TK Empirical data gathering NW, MZ NW NW, J-PB, TK, VS NW, MP TK Manuscript preparation NW NW NW NW, IH NW

J-PB = Jan-Peter Bäckman MP = Mikko Pitkänen

Supervised by Prof. Ilkka Hanski University of Helsinki Finland

Reviewed by Prof. Jari Kouki University of Joensuu Finland

Dr. Risto Väinölä University of Helsinki Finland

Examined by Prof. Michael Singer University of USA Contents 5

Contents

0. Summary ...... 7 Introduction ...... 7 Systematics and biogeography ...... 8 The relationship between melitaeines and their host ...... 11 Population structure and dynamics ...... 15 Population structure in melitaeines ...... 15 Movements of individuals ...... 18 Conclusions ...... 20 Challenges for the future ...... 21 References ...... 22 The ecology and evolution of melitaeine butterflies 7

Introduction Phylogenetical hypotheses can be used by comparative biologists to study common evo- The study of evolution is often focused on lutionary patterns across species and to infer some particular characters in a set of related which characters may have evolved in partic- species. By comparing different but related ular species as adaptations to the surrounding species one can hope to partition the effects of environment (Harvey and Pagel 1991). adaptation and constraint on a character of in- Taking a historical perspective can also help terest. The shared ancestry of species may us understand the ecology of single species confound such comparisons, but by taking living in a changing world. By comparing a into account information on the genealogical group of related species, we can identify evo- relationships of the species, one can hope to lutionary constraints on ecological features make the data conform to the assumptions of we might be interested in, such as host plant statistical analyses (Wanntorp et al. 1990; choice in butterflies. My aim in this thesis is Harvey and Pagel 1991; Harvey 1996). to make a contribution towards a better under- The comparative approach has been used standing of the evolutionary and ecological over a long period of time since Darwin patterns observable in a group of butterflies (1859) first proposed the theory of evolution belonging to the tribe Melitaeini. by natural selection. There have been two dif- Checkerspot butterflies (melitaeines) ferent traditions in the field of comparative have played a major role in helping to under- analysis, called the descent and guild tradi- stand the population biology of ever tions (Harvey and Pagel 1991). Taxonomists since Paul Ehrlich began his work on group species according to common ancestry, editha in the late 1950’s (Ehrlich while ecologists group species according to a 1961; Ehrlich et al. 1975). Work on meli- common way of life (guilds). These two tradi- taeines has been extended into many areas of tions are now being united to ask questions population biology, from population ecology about the processes of evolution. For in- and genetics to the evolution of host plant use stance, are members of a guild of species sim- and host- interactions. Most re- ilar in their ecology due to identity by descent, cently one melitaeine species, or due to parallel or convergent evolution? cinxia, has become the focal species of exten- The comparative approach is basically a sive studies on metapopulation dynamics study in adaptation. Many ecologists have no- (Hanski 1999). ticed that different species have the same ad- The melitaeines are a distinct group of but- aptations in similar environments. Different terflies in the Nymphalidae and com- species may have the same adaptations prise about 250 species (Higgins 1941, 1950, mainly for two reasons; they may share a 1955, 1960, 1981). The species are distrib- common ancestor (identity by descent) or nat- uted widely in Europe, Asia, North and South ural selection may have worked on the differ- America, but are absent from Africa south of ent species independently in a similar way the Sahara and Australia. According to the (parallel or convergent evolution) (Harvey most recent classification by Harvey (1991), and Pagel 1991). However, since the know- melitaeines form the tribe Melitaeini in the ledge of the evolutionary history of species , which includes two and species groups is at best sketchy (usually other tribes, the Nymphalini and Kallimini. the record is rather inadequate), what The Kallimini are postulated to be the sister one observes is the current state of unknown group of the Melitaeini based on larval mor- evolutionary development. In the past few de- phology (Harvey 1991) and DNA sequence cades systematic methods have enabled tax- data (Brower 2000b). onomists to build phylogenetic hypotheses The melitaeines have been taxonomically which show the best approximation of this revised extensively by L. G.Higgins over four evolutionary development for a species group decades (Higgins 1941, 1950, 1955, 1960, (Hennig 1965; Kitching et al. 1998). 1978, 1981). He divided the butterflies into 8 The ecology and evolution of melitaeine butterflies three main groups for which no morphologi- Systematics cal intermediate forms are known (Higgins and biogeography 1981). One group comprises the species be- longing to the Euphydryas, which dif- Despite the intensive taxonomic work on the fer from all other melitaeines by the structure melitaeines, nobody has attempted to build a of the genitalia and features of their life his- phylogeny for the entire group. In part this is tory. The second group is much less homoge- due to the difficulties of finding informative nous and includes melitaeine species belong- morphological characters. Many characters ing to the genera Melitaea, and 9 are invariant (which is why the group is so smaller genera. The third group consists of distinct), while the characters that vary tend to species belonging to the group, be hypervariable or form continuous clines which Higgins (1981) split into 12 genera. that make their coding very difficult (Higgins The relationships of species in this group 1941; Scott 1994, 1998). These problems of butterflies are just beginning to be discov- now have an apparently easy solution: DNA ered (I), opening up possibilities of detailed sequences (Simon et al. 1994; Caterino et al. comparative studies. The of many 2000). With the advent of the polymerase species are well known, which helps to for- chain reaction (PCR), DNA sequence data mulate relevant hypotheses that can be tested. has become accessible to just about anybody, In my thesis, I attempt to understand the eco- with the advantage that it does not require logy and evolution of melitaeine butterflies much experience to generate a large amount by investigating patterns found in a wide of data. This is in stark contrast to morpholog- range of hierarchical levels. I start from the ical data, which requires many years of expe- highest level, the level of the entire tribe, by rience for the researcher to be able to make investigating the evolutionary relationships statements of homology (Sperling 2000). of species and species groups (I). I then pro- Constructing phylogenetic trees based on ceed to use the results of (I) to infer possible DNA sequence data is not as easy as generat- evolutionary patterns in an ecological trait, ing it. The methodology of sequence analysis, the use of host plants (II). Moving down to especially for phylogenetic purposes, is in a the level of species occuring in Finland, I state of flux at the moment (Steel and Penny study the similarities and dissimilarities in 2000). There are currently three major movement patterns of five species using stan- schools of thought in sequence analysis: the dard ecological methods, but analyze these cladistic, phenetic and probabilistic schools. results with a new model (III). Related spe- Each of these promote a different way of cies tend to be similar ecologically, and I use building phylogenetic hypotheses for DNA this assumption to describe the metapopula- sequence data. The cladistic school seeks to tion dynamics of an endangered species with find a cladogram that explains the data in a information from a common related species way that minimizes the number of changes (IV). Finally, I investigate the metapopula- using the Principle of Parsimony (Farris tion dynamics of a single species in a dynamic 1970; Kitching et al. 1998) (known as the landscape and arrive at a conclusion that one maximum parsimony or MP method). The cannot rely entirely on current models to ana- phenetic school clusters those sequences that lyze the metapopulation dynamics of species are most similar to each other, usually using that inhabit dynamic landscapes (V). By us- some form of model to account for different ing comparative methods, we will eventually forms of base transformations (Saitou and be able to understand the diversity of species Nei 1987) (known as the neighbour-joining or in this tribe and perhaps be able to extend the NJ method). The probabilistic school at- results to other groups of insects. tempts to model the evolution of sequences through time, assigning each inferred change a probability and trying to find the most prob- able tree according to the given model The ecology and evolution of melitaeine butterflies 9

Euphydryas editha Figure 1. A phylo- Euphydryas phaeton genetic hypothe- Euphydryas chalcedona sis for the tribe Euphydryas colon Melitaeini based Euphydryas aurinia Euphydryiti on sequences of Euphydryas two genes in the mitochondrial ge- nome. The differ- Euphydryas maturna ent shadings on the branches Phyciodes orseis show a biogeo- Phyciodes pallida graphical hypoth- Phyciodes phaon esis for the Mel- Phyciodes tharos Phyciodes cocyta itaeini, which is Phyciodes batesii the most parsi- Phyciodes pulchella anieta monious solution ardys to optimizing dis- Anthanassa otanes Phycioditi tribution onto the Anthanassa texana Anthanassa tulcis preferred phylo- Anthanassa ptolyca genetic hypothe- pelonia Eresia eunice sis. The generic Eresia clara and subtribal Eresia burchelli classification rep- Eresia perilla Eresia plaginota resents our rec- Eresia eranites ommended clas- Eresia myia elada sification. dymas Chlosyne gaudealis Chlosyne narva Chlosyniti Chlosyne gorgone Chlosyne californica Chlosyne harrisii Chlosyne palla Chlosyne neumoegeni arachne Melitaea punica Melitaea scotosia Melitaea deserticola Melitaea latonigena Melitaea interrupta Melitaea didymoides Distribution Melitaea sutschana Melitaeiti Nearctic Melitaea cinxia Palaearctic Melitaea amoenula Neotropical Melitaea arcesia Melitaea centralasiae Melitaea deione Melitaea athalia Melitaea ambigua 10 The ecology and evolution of melitaeine butterflies

(Felsenstein 1973; Goldman 1990) (known as Penny 2000). However, to know the underly- the maximum likelihood or ML method). ing model of evolution is to know the phylo- To the novice, the choice between these genetic tree, and thus this method is best used three ways of analyzing sequence data may be to study the evolution of nucleotide se- overwhelming, and indeed many recently quences after a phylogenetic hypothesis is published papers have used all three methods available (e.g. Campbell et al. 2000). The MP and then arbitrarily chosen the results that method assumes that nature can be repre- seem the best. Some researchers advocate the sented by a hierarchical classification that can use of all three methods, claiming that if they be estimated from internested sets of syn- give the same results, one can be more confi- apomorphies (unique characters that describe dent in the conclusions (e.g. Kim 1993). a group of species) that are replicated in a However, a critical overview of all three given data set (Platnick 1979; Brower 2000a). methods shows that there are theoretical as The algorithms that have been developed to well as practical problems with some of the find such hierarchical classifications are de- methods, making their use questionable. signed to keep all the trees that explain the The NJ method has been shown to be very data equally parsimoniously. As the quality of sensitive to the order in which data are fed the data set increases, one should converge on into the algorithm, and is designed to produce the true tree. It is this method that I have cho- only one tree, regardless of the quality of the sen to use to analyze our data set (I). data (Saitou and Nei 1987; Farris et al. 1996). Once a phylogentic hypothesis is avail- This is not a desirable property as there is no able, it can be used to investigate the system- objective way to assess how well the given atics of the group in question. So far, molecu- tree is supported by the data. The ML method lar phylogenies have not been used much to has been shown to be robust and statistically test the classifications of insects that are consistent if the underlying model of evolu- based on morphological characters (Caterino tion is known (Goldman 1990; Steel and et al. 2000), though this situation is changing

Table 1. The classification of the tribe Melitaeini based in part on (I) and in part on the morphologi- cal work of Higgins (1941, 1950, 1955, 1960, 1981) and Harvey (1991).

Family Subfamily Tribe Subtribe Genus No. of species

Nymphalidae Nymphalinae Melitaeini Euphydryiti Euphydryas 14 Phycioditi Phyciodes 11 Tegosa 14 Anthanassa 27 Eresia ca 80 Phystis 1 Chlosyniti Chlosyne ca 30 Texola 1 Dymasia 1 1 Melitaeiti Melitaea ca 50 Poladryas 2 Incertae sedis Gnathotriche 5 4 Fulvia 2 2 The ecology and evolution of melitaeine butterflies 11

(e.g. Mitchell et al. 2000). Our molecular The relationship phylogeny of the Melitaeini is based on 77 between melitaeines melitaeine species and 3 outgroup species (I). and their host plants For each species we sequenced 1422 bp of the cytochrome oxidase I gene and ca. 536 bp of Phytophagous (plant-eating) insects are a the 16S ribosomal RNA gene in the mito- very species rich group of organisms (Strong chondrial genome. Our work suggests that et al. 1984) and butterflies are no exception, there are at least four groups of species that with about 20000 species described (Ackery should be given equal rank (Fig. 1). These are et al. 1999). Most phytophagous spe- the Euphydryas group (subtribe Euphydryiti), cies are highly specialized on one or a few Phyciodes group (Phycioditi), Melitaea host plant species and even the generalist spe- group (Melitaeiti) and Chlosyne group cies are not able to eat everything. These two (“Chlosyniti“). observations have intrigued researchers for The sequence divergences of the COI gen- several decades – why is phytophagy such a e were equal between the four groups of spe- successful way of living and what are the ad- cies and we could not conclusively find the vantages of specialization? The answers to relationships of the four groups. Within the these questions are just beginning to emerge, four groups, we found several genera to be but there is still much controversy about the paraphyletic, that is a given genus does not processes involved in the evolution of host describe a natural group of related species, plant use in insects (Schoonhoven et al. but includes species belonging to another ge- 1998). nus within the group. Our phylogenetic hy- In a seminal paper on insect-plant interac- pothesis is robust enough to make statements tions, Ehrlich and Raven (1964) suggested on the classification of melitaeines and we that plants evolving novel secondary com- recommend that 12 genera be synonymized pounds (chemicals thought to be involved in (I, Zimmermann et al. 2000). Though our plant defenses) are able to escape predation, phylogeny is by no means complete, espe- thus setting the stage for species radiations. cially concerning the Neotropical species of Any insect then evolving resistance to these Phycioditi, I suggest that the classification secondary compounds is confronted with an should follow that in Table 1. abundance of potential host plants and an- The molecular phylogeny has interesting other species radiation can take place. The hy- implications for the broad historical biogeo- pothesis of Ehrlich and Raven (1964) sug- graphy of the tribe (I). It would appear that the gests that there is coevolution between insects melitaeines originated in the Nearctic (Fig. and their host plants, i. e. both groups affect 1), where the basal members of all four major each other in an evolutionary context. groups are extant. The Neotropics have been Through the process of coevolution (also colonized three times, once in the Phyciodes termed an evolutionary arms race between in- group and twice in the Chlosyne group. The sects and plants), insects have become highly colonization by the ancestor of the Neotropi- specialized, with most species utilizing only cal Phyciodes clade has led to a species radia- one or a few plant species. tion, as the clade putatively contains about However, the reciprocality of the selective 120 species (only 14 species were included in responses has been questioned, based on ob- the analysis of the molecular data in I), which servations that while plants exert strong se- is almost half of all species in the Melitaeini. lective pressures on insects, insects rarely ex- The Palaearctic has been colonized twice, ert strong selective pressures on plants (Jermy once by the Euphydryas group and once by 1976, 1984; Schoonhoven et al. 1998). This the Melitaea group. There has been one observation has led to the the hypothesis of recolonization of the Nearctic in the subgenus sequential evolution, which posits that insects Hypodryas of the Euphydryas group (Zim- are merely following the evolution of plant mermann et al. 2000). secondary compound without directly affect- 12 The ecology and evolution of melitaeine butterflies

Table 2. The occurrence of iridoids in plant families used by melitaeine butterflies as host plants according to Jensen (1991).

Melitaeine Host plant of iridoids Number of melitaeine species subtribe family found known to use as hosts

Euphydryiti Scrophulariaceae iridoid glycosides 1 Plantaginaceae iridoid glycosides 7 Caprifoliaceae seco-iridoids 7 Adoxaceae seco-iridoids 1 Dipsacaceae seco-iridoids 2 Oleaceae seco-iridoids 2 Valerianaceae seco-iridoids 2 Lamiaceae iridoid glycosides 2 iridoid glycosides 5 Gentianaceae seco-iridoids 1 Chlosyniti Scrophulariaceae iridoid glycosides 1 Orobanchaceae iridoid glycosides 4 no iridoids 5 no iridoids 8 Amaranthaceae no iridoids 1 Phycioditi Verbenaceae iridoid glycosides 1 Acanthaceae no iridoids 9 Asteraceae no iridoids 9 Urticaceae no iridoids 1 Convolvulaceae no iridoids 1 Melitaeiti Scrophulariaceae iridoid glycosides 2 Plantaginaceae iridoid glycosides 14 Valerianaceae seco-iridoids 1 Lamiaceae iridoid glycosides 1 Asteraceae no iridoids 4 Orobanchaceae iridoid glycosides 1 Gentianaceae seco-iridoids 1 ing it, i. e. speciation in phytophagous insects 2000b; Angiosperm Phylogeny Group 1998). can be brought about by plants but speciation The families Scrophulariaceae, Lamiaceae, in plants is not caused by insects feeding on Plantaginaceae, Oleaceae, Acanthaceae, them. Verbenaceae, Gentianaceae, Orobanchaceae An investigation of these hypotheses re- and Convolvulaceae belong to one clade (the quires that patterns of host plant use are asterid I clade); and Asteraceae, Adoxaceae, placed in an historical perspective. In (II)I Caprifoliaceae, Valerianaceae and Dipsaca- have studied the evolutionary history of host ceae belong to the other clade (asterid II plant use in melitaeine butterflies by using the clade). The remaining two families are en- phylogenetic hypothesis from (I). Larvae of tirely unrelated to the previous families, melitaeine species are found on a rather re- Urticaceae belongs to the subclass Rosidae stricted range of host plants (II). Most species and Amaranthaceae belongs to the subclass (or populations) are oligophagous or even Caryophyllidae. Eleven of these families are monophagous on plant species belonging to united by the presence of secondary com- 16 families (Table 2). Fourteen families be- pounds known as iridoids (Jensen et al. 1975; long to the subclass Asteridae, and are found Jensen 1991). Four families, Asteraceae, in two distinct clades (Olmstead et al. 1993; Convolvulaceae, Urticaceae and Amarantha- The ecology and evolution of melitaeine butterflies 13 ceae, do not contain iridoids. The ability to sequester iridoid glycosides has The relationship between melitaeines and been recorded in 5 species of Euphdryas their host plants has been much studied since (Bowers and Puttick 1986; Stermitz et al. Singer (1971, 1983; White and Singer 1974) 1986, 1994; Franke et al. 1987; Gardner and discovered that different populations of a sin- Stermitz 1988; Belofsky et al. 1989; L’Emp- gle species Euphydryas editha preferred dif- ereur and Stermitz 1990a), 2 species of ferent host plants. Bowers (1981, 1983b) Chlosyne (Mead et al. 1993; Stermitz et al. showed that the host plants of Euphydryas 1994), Poladryas minuta (L’Empereur and species in North America all contained Stermitz 1990b) and Melitaea cinxia (Lei and iridoids. Bowers (1980, 1981) was intrigued Camara 1999). Bowers and Williams (1995) by the fact that Euphydryas larvae and adults found that though the larvae of Euphydryas are aposematically coloured and found that gillettii are found mainly on plants containing they were unpalatable and even emetic to ver- seco-iridoids, they were unable to sequester tebrate predators. The reason behind the un- these compounds. Euphydryas gillettii larvae palatability of the butterflies is the ability of were able to sequester iridoid glycosides from larvae to sequester iridoids (Bowers and other plants that postdiapause larvae some- Puttick 1986). Iridoids are known to be very times feed on. bitter tasting compounds and have been used When a historical perspective is adopted, as insecticides against generalist insect herbi- it becomes apparent that iridoid glycosides vores (Hegnauer 1964; Seigler 1998). have had a substantial impact on the evolution Iridoids have been found to be important of host plant use in melitaeine butterflies (II). feeding stimulants for Euphydryas chalce- When the presence of iridoid glycosides in dona larvae (Bowers 1983b). The larvae re- the host plants of extant melitaeine species is fused to feed on pure artificial diet, but when mapped onto the phylogeny of the butterflies, catalpol (an iridoid glycoside) was added to it can be seen that this trait is very conserva- the artificial diet, the larve fed actively tive, i. e. there does not seem to be much (Bowers 1983b). This finding led Bowers switching back and forth between character (1983b) to postulate that the ability to utilize states. In contrast, when the use of host plant iridoids by Euphydryas species has enabled families is mapped onto the phylogeny, the them to colonize a variety of plant families patterns are much more dynamic (see Fig. 3 in containing iridoids. My study (II) suggests II). The evolutionary dynamics of host plant that this hypothesis is relevant to the entire use are evident as the widening of host plant tribe of Melitaeini. range in clades using plants containing iridoid The ability of melitaeine species to se- containing plants and as host shifts to chemi- quester iridoids has been studied in several cally dissimilar plants. species. Iridoid glycosides are a diverse The patterns I have described in (II) are group of chemical compounds (over a thou- generated by the behavior of individuals over sand different compounds have been re- evolutionary time. In melitaeines it is the ovi- corded) and can be divided into two groups of positing female that is the most crucial stage compounds with similar structures. These are of host plant choice, as newly hatched larvae iridoid glycosides and seco-iridoids (Jensen are not able disperse over distances longer 1991; Seigler 1998). So far, all iridoids that than a few cm (Moore 1989). All melitaeine have been recorded to be sequesterable by species that have been studied have shown melitaeine species are iridoid glycosides similar oviposition behavior to the well-stud- (Bowers and Puttick 1986; Stermitz et al. ied Euphydryas editha (Singer 1994; Thomas 1986, 1994; Franke et al. 1987; Belofsky et al. and Singer 1998), e. g. Euphydryas maturna 1989; L’Empereur and Stermitz 1990b; Mead (Wahlberg 1998), Melitaea cinxia (Kuussaari et al. 1993; Bowers and Williams 1995). In et al. 2000) and Melitaea diamina (Wahlberg fact, there are two iridoid glycosides that are 1997). Detailed studies on the host plant pref- most often sequestered; catalpol and aucubin. erences of females have shown that the fe- 14 The ecology and evolution of melitaeine butterflies males are choosing plant individuals rather the dynamism of host plant family utilization than plant species to oviposit on (Ng 1988; in related species. It is at this level that one Singer and Lee 2000). This means that an in- should see signs of coevolution over longer dividual of one plant species may be preferred periods of time. It is very clear that parallel over an individual of another plant species, phylogenesis has not occurred in melitaeines which in turn may be more acceptable than and their host plants, as there is dynamism of another individual of the first species. This host plant utilization both at the species level implies that females are choosing to oviposit and at the clade level. Mitter and Farrell on a plant individual based on the biochemi- (1991) stress that the ages of the insect and cal profile of that plant individual. host plant clades should be similar, but most Going up from the level of the individual of the host plant families in this case are likely butterfly to a population of butterflies, we to be much older than the melitaeines, e.g. find that most females prefer to oviposit on Acanthaceae 19 My, Asteraceae 31 My, and one species of host plant (Singer et al. 1994; Caprifoliaceae 47 My (Eriksson and Bremer Kuussaari et al. 2000), indicating that bio- 1992). In (I) we speculate that the tribe chemical profiles are usually plant species Melitaeini originated at the beginning of the specific, but not always (Singer and Lee ice ages ca. 5 Mya, based on low sequence di- 2000). An environmental perturbation may vergences and the biogeography of the tribe. introduce a new plant species or change the The question then is whether the phenology of an existing plant species and the melitaeines have coevolved with their host biochemical profile of these species may be plants in a broader sense. Coevolution im- more acceptable to some ovipositing females plies that the insects should affect the fitness (Singer et al. 1993; Thomas and Singer 1998). of the host plants in a negative way. Most If the new host supports higher larval sur- Holarctic melitaeine species feed on herbs of vival, the average female preference of the small size and in some cases the larvae are population may change rapidly (Singer et al. able to kill individuals of their host plants 1993). Note that environmental perturbations (Parmesan 2000). Only one study has explic- have been common especially for Nearctic itly studied the effect of melitaeine herbivory and Palaearctic species over the past 5 My on the fitness of the host plants (Parmesan (glacial periods). 2000). This study showed a surprising result Moving up from the level of populations that when plant density was low, herbivory to an entire species (which is the smallest unit had a significant negative effect on the fitness in this study), one finds that different popula- of the host plant, but when plant density was tions have become specialized on different high, herbivory had no effect on host plant fit- host plant species usually in the same plant ness. This indicates that competition between family. This pattern is very clear in many plants may be a stronger evolutionary force Holarctic species and the apparently mono- than herbivory by insects. Also, insects are phagous Neotropical species may just repre- usually distributed patchily in the landscape sent a dearth of information from this region. and do not affect the plant population as a Within one species that has been studied whole in a certain area. Thus plants with simi- (Euphydryas editha), the evolution of host lar genotypes to those that are eaten are able to plant use appears to have been very dynamic, escape predation. This situation is common in with several host plant genera being lost and batch laying melitaeines, which are highly lo- recolonized several times by different popu- calized as larvae in a given habitat patch. lations of the butterfly (Radtkey and Singer The most likely explanation for melitaeine 1995). host plant use is that the butterflies have colo- As one moves up still further to the level of nized an already diverse assemblage of clades of species, my study (II) has shown plants. Melitaeines have not coevolved with that the apparent dynamism of host plant gen- iridoid containing plants, but rather have been era utilization within species is reflected in able to circumvent the plants’ defences and The ecology and evolution of melitaeine butterflies 15 are now able to exploit the plants. Whether in- taeines contain many compounds other than sects have been instrumental in the evolution iridoids. How sensitive melitaeines are to of iridoids has not been answered by this these other secondary compounds has not study, but that melitaeines have not been in- been studied much. Stermitz et al. (1989) re- strumental is clear. Some ancestral popula- port that quinolizidine alkaloids that the tions have specialized on plants containing hemiparasitic host plant of Euphydryas seco-iridoids in addition to those containing editha obtain from another plant, do not affect iridoid glycosides. One lineage has speciated most larvae. Some larvae are however af- to form the Euphydryas group and two lin- fected by these compounds. My study (II) has eages have not speciated (yet?). This again shown that the presence of iridoids in the host suggests that the ancestral populations have plants of melitaeines is a phylogenetically evolved a way to circumvent the negative ef- conservative character. Further research fects seco-iridoids and thus the butterflies should concentrate on finding other chemi- have merely followed the plants, rather than cals that influence host plant use in these but- caused the evolution of a more potent plant terflies. defence. There are three groups of melitaeine spe- cies that depart from the general pattern of us- ing host plants containing iridoids, and all Population structure three groups use host plants in the and dynamics Acanthaceae or Asteraceae (II), which do not contain iridoids at all (Jensen et al. 1975; Population structure in melitaeines Jensen 1991). The three groups of species are in the genera Melitaea, Chlosyne and A striking feature of melitaeine populations Phyciodes. Whether the host plants in these that was noted already at the beginning of this two families confer some sort of protection to century is their patchy nature (Ford and Ford the larvae feeding on them is still an open 1930; Ehrlich 1961). This patchiness is high- question. Adult Chlosyne harrisii were found lighted by the often very sedentary behaviour to be palatable to a bird predator (Bowers of individuals within a habitat patch (Ehrlich 1983a), while larvae of C. lacinia were found 1961, 1965; Warren 1987; Harrison 1989; to be unpalatable to amphibian predators Hanski et al. 1994). A consequence of this (Clark and Faeth 1997). Both species feed on sedentary behaviour is that populations occu- plants belonging to Asteraceae. pying different habitat patches often fluctuate In the case of the Chlosyne group, species in size independent of each other (e.g. Ehrlich ancestral to the C. nycteis clade used host et al. 1975; Ehrlich and Murphy 1981; Hanski plants in Orobanchaceae, which are hemi- et al. 1995a). Sometimes populations in cer- parasitic plant species. These plants are able tain patches may go extinct, but these extinc- to take up plant secondary compounds from tions can be balanced by occasional coloniza- their hosts (Stermitz et al. 1989). If the hosts tions of empty patches (Harrison et al. 1988; of the ancestral Orobanchaceae that the Hanski et al. 1995a). Chlosyne species fed upon were plants be- The population structure described above longing to Asteraceae, the butterfly would be is known as a metapopulation, or a population exposed to the secondary compounds of of populations (Levins 1969). Meta- Asteraceae. This may have then facilitated populations and their dynamics have become the colonization of Asteraceae. In the other very popular subjects of study recently, espe- two groups, the host plant affiliations of an- cially in butterflies (Thomas and Hanski cestral species is unclear, and thus my hy- 1997). Melitaeines are ideal subjects for pothesis remains to be tested in a more rigor- metapopulation studies mainly because suit- ous fashion. able habitat patches are usually easily delim- It is clear that the host plants of meli- ited from the surrounding habitat and the 16 The ecology and evolution of melitaeine butterflies presence or absence of a species is fairly easy lation may sometimes depend on how the two to assess (Harrison et al. 1988; Hanski et al. resources are distributed relative to each other 1995a; IV, V). (Gilbert and Singer 1973). All studied melitaeine species exhibit a Ehrlich (1961, 1965) found that an E. fragmented population structure. Such spe- editha colony inhabiting seemingly uniform cies are Euphydryas editha (Ehrlich et al. habitat was in fact highly aggregated. These 1975; Thomas et al. 1996), E. chalcedona aggregations formed three local populations (Brown and Ehrlich 1980), E. gillettii that fluctuated in size independently of each (Debinski 1994), E. anicia (White 1980), E. other (Ehrlich et al. 1975). Even though there phaeton (Brussard and Vawter 1975), E. was no physical barrier between these popu- aurinia (Warren 1994; Lewis and Hurford lations, very few butterflies moved from one 1997; V), E. maturna (III), Melitaea cinxia population to another. This observation led (Hanski et al. 1994, 1995a, 1995b, 1996), M. Ehrlich (1961) to propose some sort of “in- diamina (IV), M. didyma (Vogel 1996; Vogel trinsic barriers to dispersal”. It was later dis- and Johannesen 1996) and M. athalia (War- covered that the populations were situated in ren 1987; III). What is evident from the list places where the larvae had access to alterna- above is that the population structures of any tive host plants after the senescence of the pri- Chlosyne or Phyciodes species have not been mary host plant, thus allowing larvae to de- studied in detail. Dethier and MacArthur velop up to diapause (Singer 1972). Singer (1964) report that C. harrisii inhabits a net- (1972) proposed that individuals are selected work of old fields in a forested region, sug- for sedentary behaviour, because adult butter- gesting that this species has a metapopula- flies were unable to recognize the alternative tion. On the other hand, a mark-recapture host plant and thus suitable habitat. study on C. palla suggests that this species oc- Other populations of E. editha are found in cupies a much larger area and moves more habitats where larval host plants and adult than Euphydryas or Melitaea species (Schrier sources can occur several hundred me- et al. 1976). ters apart from each other (Gilbert and Singer Are melitaeines then more susceptible to a 1973). Adults in these populations are much metapopulation structure than other butter- more vagile, moving between both resources flies? Apparently not. The metapopulation with ease. Consequently, the area covered by structure is fairly common in butterflies local populations at these sites is much larger (Hanski and Kuussaari 1995; Thomas and than at the site described previously. Further Hanski 1997). Hanski and Kuussaari (1995) studies showed that at least one colony of E. estimated that 65% of the 94 species of butter- editha exists as a mainland-island metapopu- flies living in Finland have a metapopulation lation (Harrison et al. 1988). In this colony, structure. What characteristics in the meli- one population exists on a habitat patch with taeines can be thought to affect their popula- an area of over 2,000 ha and it numbers maxi- tion structure? There are two major factors; mally in the hundreds of thousands of individ- the occurrence of discrete local populations uals. This large local population is sur- and the magnitude of adult movements be- rounded by smaller habitat patches of which tween local populations. those closer to the “mainland“ population are What makes melitaeine local populations more likely to be occupied. The risk of extinc- discrete in space? Most studied species are tion of the mainland population is thought to found in habitats that are well separated from be minimal, while the surrounding smaller the surrounding habitat, such as open mead- populations are thought to go extinct fre- ows in a forest matrix (e.g. Warren 1987; quently. Empty habitat patches are colonized Hanski et al. 1996b; IV,V). Two important re- mainly from the mainland population (Harri- sources often occur together in such habitats, son et al. 1988). adult nectar sources and larval host plants. Many melitaeines are known to exist in The size of the area occupied by a local popu- classical metapopulations, where all local The ecology and evolution of melitaeine butterflies 17 populations have a substantial risk of extinc- of empty habitat patches is related to the con- tion (Hanski et al. 1995a; IV, V). One system nectivity of the patches. Details of the inci- has been particularly well studied at the meta- dence function model are given in (IV, V). In population level. This is the Melitaea cinxia short, the incidence function model has 5 pa- metapopulation in the Åland Islands in SW rameters that are estimated from observed Finland (Hanski et al. 1994, 1995a, 1995b, patch occupancies. The parameters describe 1996b; Hanski 1999). Melitaea cinxia inhab- the annual risk of local population , its a patch network of roughly 3,000 patches, how fast the extinction risk increases with de- of which 300 – 500 have been occupied at any creasing patch area, the effect of distance be- one time (Hanski et al. 1995a; Hanski 1999). tween patches on colonization of empty The entire network has been surveyed twice a patches, the efficiency with which coloniza- year since 1993, yielding a time series that has tions occur and the relationship between brought many insights into how meta- patch area and expected population size. To populations work. estimate parameter values for the incidence It has been shown beyond doubt that M. function model from the occupancy pattern of cinxia exists in a stochastic balance between one year, one has to assume that the meta- extinction of local populations and coloniza- population is at a stochastic steady state. This tion of empty patches (Hanski et al. 1995a; is a potentially problematic assumption for Hanski 1999). Over the years it has become endangered species, whose populations have apparent that the metapopulation on the most likely declined strongly over past years. Åland Islands actually consists of many meta- We applied the incidence function model to populations in semi-independent patch net- two endangered species, Melitaea diamina works, given the acronym SIN by Hanski et (IV) and Euphydryas aurinia (V), in order to al. (1996). The metapopulations in these SINs assess their in Finland. fluctuated independently of each other, but In the case of M. diamina, we investigated there appears to be some gene flow between how well the parameter values of three differ- them (I. Saccheri, pers. comm.). Semi-inde- ent species of butterfly were able to predict pendent patch networks have been recorded the observed occupancy pattern of the endan- in M. diamina as well (IV). gered species (IV). The best results were Other species have also been studied in the given by the parameter values for the most metapopulation perspective. Melitaea di- closely related species, M. cinxia. Our study dyma occurs as a metapopulation at the north- draws attention to the historical component in ern edge of its range in Germany (Vogel1996; the ecologies of different species. The most Vogeland Johannesen 1996). The species ap- likely reason why our study was successful is parently occupied all the suitable habitat that the two species M. diamina and M. cinxia available, as no or colonizations share a relatively recent ancestor. This im- were observed. The same appears to be true plies that there are constraints on the evolu- for Finnish populations of M. athalia and tion of ecological parameters such as move- E. maturna (III). In these species suitable ment ability (III). Our study represents the habitats occur quite densely, so even though first attempt in what promises to be an intrigu- the butterflies are not more mobile than M. ing area of research, comparative metapopu- cinxia (III), they occupy almost all available lation biology. A rigorous approach is needed habitat. to investigate whether some aspects of the The dynamics of species inhabiting frag- ecology of species living in a fragmented mented landscapes have been successfully landscape are constrained by phylogeny, and analyzed using a stochastic model known as which features are free to evolve in a chang- the incidence function model (Hanski 1994). ing world. The incidence function model assumes that In most studies of metapopulations, the the extinction risk of a local population is re- habitat patch network is assumed to be static, lated to the patch area, and that colonization i. e. the quality of patches does not change 18 The ecology and evolution of melitaeine butterflies with time and patches do not disappear. How- larval host plants in the landscape. Whether ever, butterflies often inhabit successional all suitable habitat patches are occupied or habitats and their patch networks are there- whether the species in question exists in a sto- fore dynamic, with patches appearing and chastic balance between extinctions and colo- disappearing in the landscape. Our study of E. nizations depends on the spatial configuration aurinia is a good example of such a system of the patches and on their number. The prob- (V). This species lives in a patch network of able situation is that in the central parts of a and small-scale clearcuts in the for- species’ distribution, suitable habitat patches est. The meadows can be considered to be are numerous and relatively close to each static, though currently they are becoming other. As one moves towards the edge of a overgrown due to changes in agricultural species’ range, the patch network becomes practices. Clearcuts are distinctly transient less dense and the occurrence of a species be- habitat patches, being suitable for at most 12 comes more dependent on metapopulation years. The same approach to analyzing the processes (Thomas et al. 1998). Some rare or dynamics of E. aurinia as was used in (IV) endangered species may be entirely depend- does not work in this case as the fundamental ent on metapopulation processes, as is the assumptions (see above) of the incidence case with M. diamina in Finland (IV). function model are violated. In dynamic patch networks, the presence of a species may be a reflection of the history of the surround- Movements of individuals ing landscape and extinctions can be deter- ministic rather than stochastic. Movements of melitaeine butterflies have Since the modelling approach to meta- been much investigated using mark-recapture populations inhabiting dynamic patch net- studies, beginning with the seminal work of works is still undeveloped, we analyzed the Ehrlich (1961, 1965). Most studies have dynamics of E. aurinia in its patch network in found melitaeines to be fairly sedentary, re- a somewhat ad hoc manner (V). We manually gardless of how common or rare they are adjusted the parameter values of the inci- (Ehrlich 1965; Schrier et al. 1976; Cul- dence function model to give an average inci- lenward et al. 1979; Brown and Ehrlich 1980; dence, similar to that observed in the field, in Warren 1987; Hanski et al. 1994; Vogel1996; a dynamic landscape that we attempted to Munguira et al. 1997). Due to this sedentary make as realistic as possible. With this ap- behaviour, populations of the butterflies have proach we discovered that the meadows are been referred to as “closed populations” essential to the survival of E. aurinia in SE (Thomas 1984; Warren 1992). A comparison Finland. Our study (V) highlights the need for between E. editha and Erebia epipsodea,a a theoretical framework to be developed for butterfly with an “open population structure“, the study of dynamic populations in a dy- showed that the former moved much less and namic landscape. This is especially important shorter distances than the latter (Brussard and for butterflies as most endangered species in- Ehrlich 1970). habit early successional habitats (Thomas Hanski et al. (1994) found that the division 1993). Indeed, several melitaeines are known of butterfly population structures into open to inhabit early successional habitat, e. g. M. and closed based on movements was unsatis- diamina (IV), M. athalia (Warren 1991), E. factory. They proposed that population struc- gillettii (Williams 1988) and E. maturna ture should be based on whether suitable hab- (Wahlberg 1999). itats are discrete entities in a matrix of unsuit- It appears that at least for Melitaea and able habitat and on the magnitude of move- Euphydryas species a patchy population ments of the adult butterflies. Discrete habitat structure is ubiquitous. This is not an intrinsic patches of similar size and infrequent move- feature of the butterflies, however, but is ments between patches leads to a classical largely dependent on the distribution of the metapopulation, while diffuse habitat and The ecology and evolution of melitaeine butterflies 19 vagile behaviour leads to a large panmictic Levin 1981; Murphy and White 1984). population. The sedentary behaviour of Other factors affecting emigration are the melitaeines predisposes them to a classical area of habitat patches, the quality of the metapopulation structure. patch boundary, the density of the local popu- Yet, despite their sedentary behaviour, lation and the size of the butterfly individual movements of over a kilometer have been re- (Kuussaari et al. 1996). To grossly simplify corded in all studied species (Ehrlich et al. the case, large butterflies tend to leave small 1975; Hanski et al. 1994; Hanski and patches with open boundaries and low density Kuussaari 1995; III). Movements of this of other individuals. A negatively density-de- magnitude are however rare and it has been pendent emigration rate has been found in E. questioned whether they contribute at all to editha (Gilbert and Singer 1973), E. chalce- gene flow between populations (Ehrlich et al. dona (Brown and Ehrlich 1980) and M. cinxia 1975). Ehrlich et al. based their scepticism on (Kuussaari et al. 1996). The effect of the size one metapopulation of E. editha, where off- of a butterfly has only been studied in M. spring of migrants have a very low probabil- cinxia, where it was found that larger females ity of survival. This is because migration gen- were more likely to emigrate than small ones erally happens later in the flight season and (Kuussaari et al. 1996). larvae of later egg batches are faced with the Factors affecting immigration have not senesence of the host plant before they have been studied in great detail. Kuussaari et al. reached diapause size. (1996) found that butterflies were more likely The unimportance of long distance mi- to immigrate into larger patches close to ex- grants cannot be generalized to other E. isting populations. A similar pattern has been editha populations, much less to all meli- found in the surveys of the M. cinxia meta- taeine species. In most species the population, as larger and less isolated patches occassional long-distance migrant tends to are more likely to be colonized (Hanski et al. lead to less genetic differentiation in local 1995a). These effects of patch area and con- populations. This has been observed in many nectivity have been found in other species of melitaeines (Brussard and Vawter 1975; butterfly as well (Thomas and Hanski 1997). McKechnie et al. 1975; Vawter and Brussard One major factor affecting the evolution 1975; Brussard et al. 1989; Debinski 1994; of the propensity of an individual to emigrate Johannesen et al. 1996). Long-distance mi- has until recently eluded researchers. This gration has also important impacts on meta- factor is mortality during migration. If mor- population dynamics. For instance, M. cinxia tality during migration is high, selection pres- has been observed to colonize empty patches sures should be for sedentary behaviour; up to 5 km from the nearest occupied patches where as if mortality during migration is low, (Hanski 1999). Long-distance migration can there should be no barriers to wide ranging help stabilize metapopulation dynamics. migration behaviour. It is not known just how What factors affect the emigration of a evolutionarily labile the propensity to migrate butterfly individual? The quality of the habi- is. Melitaeines appear to be a remarkably ho- tat patch is evidently an important factor mogenous group when it comes to migration (White and Levin 1981; Murphy and White behaviour. Is this because all studied species 1984; Thomas and Singer 1987; Kuussaari et happen to inhabit similar patch networks or is al. 1996). Butterflies tend to leave patches there a phylogenetic component to the pro- that have less nectar sources (Kuussaari et al. pensity to migrate? 1996) and do not have the preferred host plant The best way to approach this question is (Thomas and Singer 1987). Also temporal to compare different species. Previous com- variation in habitat quality affects butterfly parisons between species have been hindered movements. Butterflies were more likely to by ad hoc methods of analyzing mark-recap- emigrate from habitat patches that were more ture data that are difficult to compare. Re- susceptible to drought in dry years (White and cently a new model (the VM model) has been 20 The ecology and evolution of melitaeine butterflies developed for the purpose of analyzing mark- in isolation and some results would be better recapture data from several patches (Hanski understood if a phylogenetic perspective et al. 2000). The parameters of this model de- would be adopted. Now that a reasonable scribe daily survival probabilities within a phylogenetical hypothesis is available for the habitat patch and during migration, emigra- group (I), the population biology of these spe- tion propensity, the scaling of patch area to cies can be studied at even greater depth. emigration and immigration and the effect of The evolution of host plant use in the distance on migration. The parameter values melitaeines lends itself readily to compara- obtained with the VM model are comparable. tive analyses, because the basic data are avail- Using the VM model, we found that five spe- able for a wide range of species (II). Though cies of melitaeines in Finland are more simi- individual species may show extreme lability lar to each other than any is to other unrelated in the use of host plant species (e.g. Radtkey species (III). A closer look at the five species and Singer 1995), the group as a whole ap- reveals some variation at a finer level. For in- pears to be mainly restricted to plants contain- stance E. aurinia tends to move further than ing iridoids. The butterflies can be seen to be E. maturna and M. cinxia females have a labile in host plant use at a small phylogenetic greater propensity to emigrate than all the scale, while being conservative at a large other species and sexes. The parameter values phylogenetic scale. The current evidence we estimated for each species and sex pre- points to three major independent coloniza- dicted that about 10–20% of migration events tions of plants without iridoids within the failed. melitaeines. Almost all the host plants with- Our study shows that while there is no out iridoids belong to Acanthaceae and phylogenetic component at the level of the Asteraceae, which are closely related to the five species, there may be phylogenetic con- other host plant families, suggesting that straints on the magnitude of migration dis- there may be a possiblity for preadaptation to tances in the group as a whole (III). Meli- some other compound(s) common to all (or taeines are known to be rather sedentary and some) of the host plant families. indeed there are no records of melitaeines mi- Comparing the population structures and grating very long distances, unlike for species movements of different species can greatly in the closely related Nymphalini (such as advance our understanding of species inhab- atalanta, Cynthia cardui and Inachis iting highly fragmented landscapes. Our stud- io). A more extensive comparative study is ies (III, IV,V) represent only an indication of needed to discover whether there are limits to this potential. By taking history into account the migration behaviour of melitaeines. Such one can infer the lability and limits of traits as- a study is now possible as the VM model sociated with movements of individuals in makes different studies more comparable. their landscape. This kind of information is relevant to conservation. Finding that the movement abilities are free to evolve within certain limits in a group of related species Conclusions would lead to different conclusions than find- ing that different clades have their own dis- I have attempted to show in this thesis how tinct limits within the broader limits for the knowledge of phylogeny can be used to eluci- whole group. The former finding would sug- date patterns of evolution in a group of spe- gest that species are able to respond quickly to cies. The melitaeines are highly suitable for changes in the landscape, while the latter comparative studies. They are a relatively would suggest that species are more con- small group of species (ca. 250 species) that strained by phylogeny and may respond to are relatively similar in many respects, yet changes in the landscape by going extinct. We vary in interesting ways in other respects. Pre- were able to study so few species that no defi- viously melitaeine species have been studied nite conclusions can be drawn, but there do The ecology and evolution of melitaeine butterflies 21 appear to be limits to movement ability within dynamics of the landscape itself and the influ- which melitaeines evolve (III). ence of this on the evolution of melitaeines. Two factors may explain the predisposi- Many aspects of melitaeine life history show tion of melitaeines to exhibit a metapopula- interesting variation that could be profitably tion structure, phylogenetic constraints on the studied by applying the comparative ap- range of movement abilities in melitaeines proach. and the patchy nature of their habitats. If there Variation in larval group size in the meli- truly are phylogenetic constraints, knowledge taeines promises to be a rich area for compar- of the configuration of the patch network may ative studies. All melitaeine species that have be enough to predict the occurrence of a been studied lay their eggs in batches. Some melitaeine species in that network (IV). Com- species lay their eggs in large batches of over mon species would thus inhabit a dense net- 300 eggs while others lay eggs in batches of work of habitat patches, while rare species less than 10 eggs. Factors affecting the evolu- would live in sparse patch networks. The tion of clutch size in different species have yet magnitude of “dense” and “sparse” would be to be analyzed. There are certainly complex similar in all species. Once again our studies interactions between larvae and the biotic and represent just the beginning. A comprehen- abiotic environment. For some species larval sive research program in comparative meta- host plant defences may be a crucial selective population biology would be needed to test factor, in others thermoregulation may be im- the above hypothesis. portant and in yet others avoidance of Our study on E. aurinia (V) highlights the may play an important role. The need to consider other characteristics of the relationship between web-spinning and habitat patch network rather than just the area group size is unknown at the moment. It may and location of each patch. The host plants of be that in species for which a web is impor- most temperate melitaeines are small herbs tant, a larger group size is advantageous, as it that tend to be found in early successional lowers the per capita cost of spinning the web. habitats. This suggests that historically the A correlation between web spinning ability evolution of melitaeine movement abilities and egg batch size would support this hypoth- has been influenced by dynamic landscapes. esis. The study of the dynamics of melitaeine The coevolution of melitaeines and their metapopulations in dynamic landscapes is in parasitoids is another potential topic for com- its infancy and our study along with that of parative studies. All recorded parasitoids are Warren (1991) serve to bring attention to this apparently specialists of melitaeines. Some phenomenon. It is not possible at this moment species are, however, generalists within the to say anything about the general implications melitaeines, while others are specialists on of dynamic landscapes on the evolution of only one melitaeine species. Parasitoids may melitaeines. be a selective factor on the behaviour of but- terfly larvae. It may be that melitaeine species that live solitarily as larvae do not have highly specialized parasitoids as the host larvae are Challenges for the future difficult for the parasitoids to find. On the other hand, extreme specialization by The above paragraphs bring forth areas of re- parasitoids may set the stage for stepwise co- search that would confirm, strengthen or pos- evolution between the parasitoids and their sibly refute the results obtained so far. To reit- hosts. A phylogeny of both groups is neces- erate, the metapopulation structures of many sary to investigate this possibility. species should continue to be studied espe- Finally, with a reliable phylogeny of the cially with reference to the movement abili- tribe Melitaeini available, this group of but- ties of each species in their respective land- terflies has the potential to become a model scapes. More attention should be paid to the group of insects in evolutionary and popula- 22 The ecology and evolution of melitaeine butterflies tion biology. Much is already known about returned me to Earth on many occassions and have many species, and placing this knowledge given me a new perspective on life. My thesis work into a historical perspective can help us un- has been funded by many instances: WWF of Fin- derstand many aspects of evolution of life his- land, the City of Tampere, VR-Yhtymät, Metsän- tory traits. tutkimuslaitos, the University of Helsinki, the Jenny and Antti Wihurin Säätiö, but the majority of the Acknowledgments funding was provided by the Academy of Finland This thesis is the outcome of interactions with many (Grant Nos. 38604 and 44887 to I. Hanski). Finally, I people that have influenced my thoughts in many would like to extend my thanks to all the world’sam- ways. First and foremost I would like to warmly ateur and professional lepidopterists whose altruism thank my supervisor Ilkka Hanski for supporting me has overwhelmed me. I hope I have not let them throughout my PhD studies. He has given me the down. freedom to wander along my own paths, yet has al- ways been interested in my research, offering help whenever I needed it. I hope I have learned the most important lesson Ilkka can have taught me: how to do References excellent quality science. The Metapopulation Re- search Group has been a very stimulating group to Ackery, P.R., R. de Jong, and R. I. Vane-Wright. 1999. work in and the environment created by the many The butterflies: Hedyloidea, Hesperoidea and members has made me feel proud to have been a part . Pp. 263–300 in N. P. Kristensen, of it. Mikko Kuussaari was the one to place my ed. Lepidoptera, Moths and Butterflies. 1. Evolu- tion, Systematics and Biogeography. Handbook searching feet on the path to becoming a lepidopter- of Zoology 4 (35), Lepidoptera. de Gruyter, ist. I can only hope that I can make field notes as me- Berlin. ticulously as he. Atte Moilanen has patiently ex- Angiosperm Phylogeny Group. 1998. An ordinal plained to me how the models I have used work, sev- classification for the families of flowering plants. eral times, something I am grateful for. I am also Annals of the Missouri Botanical Garden 85:531– pleased to acknowledge my various co-authors and 553. friends who have helped out in field and lab work. Belofsky, G., M. D. Bowers, S. Janzen, and F. Stermitz. 1989. Iridoid glycosides of Aureolaria The Division of Population Biology has been like a flava and their sequestration by Euphydryas pha- second home to me and the easiness with which I eton butterflies. Phytochemistry 28:1601–1604. have been able to interact with others at the Division Bowers, M. D. 1980. Unpalatability as a defense strat- has been very pleasant. I would especially like to egy of Euphydryas phaeton (Lepidoptera: thank Sirkka-Liisa Nyeki for always cheerfully find- Nymphalidae). Evolution 34:586–600. ing even the most obscure articles that I have asked Bowers, M. D. 1981. Unpalatability as a defense strat- egy of western checkerspot butterflies (Euphy- about. Three people have been instrumental in mak- dryas Scudder, Nymphalidae). Evolution 35:367– ing me the biologist I am today. My mother Sikku 375. Wahlberg bolstered my interest in bugs and plants Bowers, M. D. 1983a. Mimicry in North American ever since I was a toddler, my grandfather Harri checkerspot butterflies: Euphydryas phaeton and Willamo taught me to take a scientific interest in the Chlosyne harrisii (Nymphalidae). Ecological En- natural world and my uncle Heikki Willamo has con- tomology 8:1–8. Bowers, M. D. 1983b. The role of iridoid glycosides stantly reminded me that there is something mysteri- in host-plant specificity of checkerspot butter- ous in nature that makes it unbelievably beautiful. I flies. Journal of Chemical Ecology 9:475–493. am grateful to both of my parents for always being Bowers, M. D., and G. M. Puttick. 1986. Fate of in- supportive of my decisions in life. As the most spe- gested iridoid glycosides in lepidopterous herbi- cial person in my life, my wife Hanna has endured vores. Journal of Chemical Ecology 12:169–178. private lectures as I have tried to clear up some con- Bowers, M. D., and E. H. Williams. 1995. Variable chemical defence in the checkerspot butterfly cepts to myself, ravings when I’ve gotten cool results Euphydryas gillettii (Lepidoptera: Nymphalidae). and cursing when things haven’t gone as well as they Ecological Entomology 20:208–212. should have. Her support has been indispensable and Brower, A. V. Z. 2000a. Evolution is not a necessary her love has kept me going. Saara and Tommi have assumption of cladistics. Cladistics 16:143–154. The ecology and evolution of melitaeine butterflies 23

Brower, A. V. Z. 2000b. Phylogenetic relationships plants: a study in coevolution. Evolution 18:586– among the Nymphalidae (Lepidoptera), inferred 608. from partial sequences of the wingless gene. Pro- Ehrlich, P. R., R. R. White, M. C. Singer, S. W. ceedings of the Royal Society of London Series B McKechnie, and L. E. Gilbert. 1975. Checkerspot Biological Sciences 267:1201–1211. butterflies: a historical perspective. Science 188: Brown, I. L., and P. R. Ehrlich. 1980. Population bio- 221–228. logy of the checkerspot butterfly, Euphydryas Eriksson, O., and B. Bremer. 1992. Pollination sys- chalcedona: structure of the Jasper Ridge colony. tems, dispersal modes, life forms, and diversifica- Oecologia 47:239–251. tion rates in angiosperm families. Evolution Brussard, P. F., J. F. Baughman, D. D. Murphy, P. R. 46:258–266. Ehrlich, and J. Wright. 1989. Complex population Farris, J. S. 1970. Methods for computing Wagner differentiation in checkerspot butterflies trees. Systematic Zoology 19:83–92. (Euphydryas spp.). Canadian Journal of Zoology Farris, J. S., V. A. Albert, M. Källersjö, D. Lipscomb, 67:330–335. and A. G. Kluge. 1996. Parsimony jackknifing Brussard, P. F., and P. R. Ehrlich. 1970. Contrasting outpreforms neighbor-joining. Cladistics 12:99– population biology of two species of butterfly. Na- 124. ture 227:91–92. Felsenstein, J. 1973. Maximum likelihood and mini- Brussard, P. F., and A. T. Vawter. 1975. Population mum-steps methods for estimating evolutionary structure, gene flow and natural selection in popu- trees from data on discrete characters. Systematic lations of Euphydryas phaeton. Heredity 34:407– Zoology 22:240–249. 415. Ford, H. D., and E. B. Ford. 1930. Fluctuation in num- Campbell, D. L., A. V. Z. Brower, and N. E. Pierce. bers, and its influence on variation, in Melitaea 2000. Molecular evolution of the wingless gene aurinia, Rott. (Lepidoptera). Transactions of the and its implications for the phylogenetic place- Entomological Society of London 78:345–351. ment of the butterfly family Riodinidae Franke, A., H. Rimpler, and D. Schneider. 1987. (Lepidoptera: Papilionoidea). Molecular Biology Iridoid glycosides in the butterfly Euphydryas and Evolution 17:684–696. cynthia (Lepidoptera, Nymphalidae). Phyto- Caterino, M. S., S. Cho, and F. A. H. Sperling. 2000. chemistry 26:103–106. The current state of insect molecular systematics: Gardner, D. R., and F. R. Stermitz. 1988. Host plant a thriving Tower of Babel. Annual Review of En- utilization and iridoid glycoside sequestration by tomology 45:1–54. Euphydryas anicia (Lepidoptera: Nymphalidae). Clark, B. R., and S. H. Faeth. 1997. The consequences Journal of Chemical Ecology 14:2147–2168. of larval aggregation in the butterfly Chlosyne Gilbert, L. E., and M. C. Singer. 1973. Dispersal and lacinia. Ecological Entomology 22:408–415. geneflow in a butterfly species. American Natu- Cullenward, M. J., P. R. Ehrlich, R. R. White, and C. ralist 107:58–72. E. Holdren. 1979. The ecology and population ge- Goldman, N. 1990. Maximum likelihood inference of netics of an alpine checkerspot butterfly, phylogenetic trees, with special reference to a Euphydryas anicia. Oecologia 38:1–12. Poisson process model of DNAsubstitution and to Darwin, C. 1859. On the Origin of Species by Means parsimony analyses. Systematic Biology 39:345– of Natural selection, or, the Preservation of Fa- 361. voured Races in the Struggle for Life. John Hanski, I. 1994. A practical model of metapopulation Murray, London. dynamics. Journal of Ecology 63:151– Debinski, D. M. 1994. Genetic diversity assessment in 162. a metapopulation of the butterfly Euphydryas Hanski, I. 1999. Metapopulation Ecology. Oxford gillettii. Biological Conservation 70:25–31. University Press, Oxford. Dethier, V. G., and R. H. MacArthur. 1964. A field’s Hanski, I., J. Alho, and A. Moilanen. 2000. Estimating capacity to support a butterfly population. Nature the parameters of survival and migration of indi- 201:728–729. viduals in metapopulations. Ecology 81:239–251. Ehrlich, P. R. 1961. Intrinsic barriers to dispersal in Hanski, I., and M. Kuussaari. 1995. Butterfly meta- checkerspot butterfly. Science 134:108–109. population dynamics. Pp. 149–171 in N. Cappuc- Ehrlich, P.R. 1965. The population biology of the but- cino and P. W. Price, eds. Population Dynamics: terfly, Euphydryas editha. II. The structure of the New Approaches and Synthesis. Academic Press, Jasper Ridge colony. Evolution 19:327–336. San Diego, CA. Ehrlich, P. R., and D. D. Murphy. 1981. The popula- Hanski, I., M. Kuussaari, and M. Nieminen. 1994. tion biology of checkerspot butterflies Metapopulation structure and migration in the (Euphydryas). Biologisches Zentralblatt 100: butterfly Melitaea cinxia. Ecology 75:747–762. 613–629. Hanski, I., A. Moilanen, T. Pakkala, and M. Ehrlich, P. R., and P. H. Raven. 1964. Butterflies and Kuussaari. 1996. The quantitative incidence func- 24 The ecology and evolution of melitaeine butterflies

tion model and persistence of an endangered but- History 43:77–243. terfly metapopulation. Conservation Biology Jensen, S. R. 1991. Plant iridoids, their biosynthesis 10:578–590. and distribution in angiosperms. Pp. 133–158 in J. Hanski, I., T. Pakkala, M. Kuussaari, and G. Lei. B. Harborne and F. A. Tomas–Barberan, eds. Eco- 1995a. Metapopulation persistence of an endan- logical Chemistry and Biochemistry of Plant gered butterfly in a fragmented landscape. Oikos Terpenoids. Clarendon Press, Oxford. 72:21–28. Jensen, S. R., B. J. Nielsen, and R. Dahlgren. 1975. Hanski, I., J. Pöyry, T. Pakkala, and M. Kuussaari. Iridoid compounds, their occurrence and system- 1995b. Multiple equilibria in metapopulation dy- atic importance in the angiosperms. Botanisk namics. Nature 377:618–621. Notiser 128:148–180. Harrison, S. 1989. Long-distance dispersal and colo- Jermy, T. 1976. Insect–host–plant relationship – co- nization in the bay checkerspot butterfly, evolution or sequential evolution? Symposia Euphydryas editha bayensis. Ecology 70:1236– Biologica Hungarica 16:109–113. 1243. Jermy, T. 1984. Evolution of insect/host plant rela- Harrison, S., D. D. Murphy, and P. R. Ehrlich. 1988. tionships. American Naturalist 124:609–630. Distribution of the bay checkerspot butterfly, Johannesen, J., M. Veith, and A. Seitz. 1996. Popula- Euphydryas editha bayensis: Evidence for a meta- tion genetic structure of the butterfly Melitaea population model. American Naturalist 132:360– didyma (Nymphalidae) along a northern distribu- 382. tion range border. Molecular Ecology 5:259–267. Harvey, D. J. 1991. Higher classification of the Kim, J. 1993. Improving the accuracy of phylogenetic Nymphalidae, Appendix B. Pp. 255–273 in H. F. estimation by combining different methods. Sys- Nijhout, ed. The Development and Evolution of tematic Biology 42:331–340. Butterfly Wing Patterns. Smithsonian Institution Kitching, I. J., P. L. Forey, C. J. Humphries, and D. M. Press, Washington DC. Williams. 1998. Cladistics. Second Edition. The Harvey, P. H. 1996. Phylogenies for ecologists. Jour- Theory and Practice of Parsimony Analysis. Ox- nal of Animal Ecology 65:255–263. ford University Press, Oxford. Harvey, P. H., and M. D. Pagel. 1991. The Compara- Kuussaari, M., M. Nieminen, and I. Hanski. 1996. An tive Method in Evolutionary Biology. Oxford experimental study of migration in the Glanville University Press, Oxford. fritillary butterfly Melitaea cinxia. Journal of Ani- Hegnauer, R. 1964. Chemotaxonomie der Pflanzen mal Ecology 65:791–801. III. Birkhäuser Verlag, Basel. Kuussaari, M., M. Singer, and I. Hanski. 2000. Local Hennig, W. 1965. Phylogenetic systematics. Annual specialization and landscape–level influence on Review of Entomology 10:97–116. host use in an herbivorous insect. Ecology Higgins, L. G. 1941. An illustrated catalogue of the 81:2177–2187. Palearctic Melitaea (Lep. Rhopalocera). Transac- Lei, G.-C., and M. D. Camara. 1999. Behaviour of a tions of the Royal Entomological Society of Lon- specialist parasitoid, Cotesia melitaearum: from don 91:175–365. individual behaviour to metapopulation pro- Higgins, L. G. 1950. A descriptive catalogue of the cesses. Ecological Entomology 24:59–72. Palearctic Euphydryas (Lepidoptera: Rhopalo- L’Empereur, K. M., and F. R. Stermitz. 1990a. Iridoid cera). Transactions of the Royal Entomological glycoside content of Euphydryas anicia Society of London 101:435–487. (Lepidoptera: Nymphalidae) and its major host Higgins, L. G.1955. Adescriptive catalogue of the ge- plant, Besseya plantaginea (Scrophulariaceae), at nus Mellicta Billberg (Lepidoptera: Nympha- a high plains Colorado site. Journal of Chemical lidae) and its species, with supplementary notes Ecology 16:187–197. on the genera Melitaea and Euphydryas. Transac- L’Empereur, K. M., and F. R. Stermitz. 1990b. Iridoid tions of the Royal Entomological Society of Lon- glycoside metabolism and sequestration by don 10:61–127. Poladryas minuta (Lepidoptera: Nymphalidae) Higgins, L. G. 1960. A revision of the melitaeine ge- feeding on Penstemon virgatus (Scrophu- nus Chlosyne and allied species (Lepidoptera: lariaceae). Journal of Chemical Ecology Nymphalinae). Transactions of the Royal Ento- 16:1495–1506. mological Society of London 112:381–465. Levins, R. 1969. Some demographic and genetic con- Higgins, L. G. 1978. A revision of the genus sequences of environmental heterogeneity for bi- Euphydryas Scudder (Lepidoptera: Nympha- ological control. Bulletin of the Entomological lidae). Entomologist’s Gazette 29:109–115. Society of America 15:237–240. Higgins, L. G. 1981. A revision of Phyciodes Hübner Lewis, O. T., and C. Hurford. 1997. Assessing the sta- and related genera, with a review of the classifica- tus of the marsh fritillary butterfly (Eurodryas tion of the Melitaeinae (Lepidoptera: Nympha- aurinia): an example from Glamorgan, UK. Jour- lidae). Bulletin of the British Museum of Natural nal of Insect Conservation 1:159–166. The ecology and evolution of melitaeine butterflies 25

McKechnie, S. W., P. R. Ehrlich, and R. R. White. Evolution. Chapman & Hall, London. 1975. Population genetics of Euphydryas butter- Schrier, R. D., M. J. Cullenward, P. R. Ehrlich, and R. flies. I. Genetic variation and the neutrality hy- R. White. 1976. The structure and genetics of a pothesis. Genetics 81:571–594. montane population of the checkerspot butterfly, Mead, E. W., T. A. Foderaro, D. R. Gardner, and F. R. Chlosyne palla. Oecologia 25:279–289. Stermitz. 1993. Iridoid glycoside sequestration by Scott, J. A. 1994. Biology and systematics of Thessalia leanira (Lepidoptera: Nymphalidae) Phyciodes (Phyciodes). Papilio (New Series) 7:1– feeding on integra (Scrophulariaceae). 120 (privately published, available from author). Journal of Chemical Ecology 19:1155–1166. Scott, J. A. 1998. Phyciodes (Phyciodes): new discov- Mitchell, A., C. Mitter, and J. C. Regier. 2000. More eries, new subspecies, and convergence. Papilio taxa or more characters revisited: combining data (New Series) 10:1–42 (privately published, avail- from nuclear protein-encoding genes for phylo- able from author). genetic analyses of Noctuoidea (Insecta: Lepi- Seigler, D. S. 1998. Plant Secondary Metabolism. doptera). Systematic Biology 49:202–224. Kluwer Academic Publishers, Norwell, MA. Moore, S. D. 1989. Patterns of juvenile mortality Simon, C., F. Frati, A. Beckenbach, B. Crespi, H. Liu, within an oligophagous insect population. Eco- and P. Flook. 1994. Evolution, weighting, and logy 70:1726–1737. phylogenetic utility of mitochondrial gene se- Munguira, M. L., J. Martin, E. Garcia Barros, and L. quences and a compilation of conserved polymer- Viejo Jose. 1997. Use of space and resources in a ase chain reaction primers. Annals of the Entomo- Mediterranean population of the butterfly logical Society of America 87:651–701. Euphydryas aurinia. Acta Oecologica 18:597– Singer, M. C. 1971. Evolution of food-plant prefer- 612. ence in the butterfly Euphydryas editha. Evolu- Murphy, D. D., and R. R. White. 1984. Rainfall, re- tion 25:383–389. sources, and dispersal in southern populations of Singer, M. C. 1972. Complex components of habitat Euphydryas editha (Lepidoptera: Nymphalidae). suitability within a butterfly colony. Science Pan-Pacific Entomologist 60:350–354. 176:75–77. Ng, D. 1988. A novel level of interactions in plant-in- Singer, M. C. 1983. Determinants of multiple host use sect systems. Nature 334:611–613. by a phytophagous insect population. Evolution Olmstead, R. G., B. Bremer, K. M. Scott, and J. D. 37:389–403. Palmer. 1993. A parsimony analysis of the Singer, M. C. 1994. Behavioral constraints on the evo- Asteridae sensu lato based on rbcL sequences. lutionary expansion of insect diet: a case history Annals of the Missouri Botanical Gardens from checkerspot butterflies. Pp. 279–296 in L. 80:700–722. Real, ed. Behavioral Mechanisms in Evolutionary Olmstead, R. G., C. W. dePamphilis, A. D. Wolfe, N. Ecology. University of Chicago Press, Chicago. D. Young, W. J. Elisons, and P. A. Reeves. 2000a. Singer, M. C., and J. R. Lee. 2000. Discrimination Disintegration of the Scrophulariaceae. American within and between host species by a butterfly: Journal of Botany 87:in press. implications for design of preference experi- Olmstead, R. G., K.-J. Kim, R. K. Jansen, and S. J. ments. Ecology Letters 3:101–105. Wagstaff. 2000b. The phylogeny of the Asteridae Singer, M. C., C. D. Thomas, H. L. Billington, and C. sensu lato based on chloroplast ndhF gene se- Parmesan. 1994. Correlates of speed of evolution quences. Molecular Phylogenetics and Evolution of host preference in a set of twelve populations of 16:96–112. the butterfly Euphydryas editha. Ecoscience Parmesan, C. 2000. Unexpected density-dependent 1:107–114. effects of herbivory in a wild population of the an- Singer, M. C., C. D. Thomas, and C. Parmesan. 1993. nual Collinsia torreyi. Journal of Ecology Rapid human-induced evolution of insect-host as- 88:392–400. sociations. Nature 366:681–683. Platnick, N. I. 1979. Philosophy and the transforma- Sperling, F. 2000. Butterfly species and molecular tion of cladistics. Systematic Zoology 28:537– phylogenies. Pp. in press in C. Boggs, W. Watt and 546. P. Ehrlich, eds. Ecology and Evolution Taking Radtkey, R. R., and M. C. Singer. 1995. Repeated re- Flight: Butterflies as Model Study Systems. Uni- versals of host-preference evolution in a specialist versity of Chicago Press, Chicago. insect herbivore. Evolution 49:351–359. Steel, M., and D. Penny. 2000. Parsimony, likelihood, Saitou, N., and M. Nei. 1987. The neighbor-joining and the role of models in molecular method: a new method for reconstructing phylo- phylogenetics. Molecular Biology and Evolution genetic trees. Molecular Biology and Evolution 17:839–850. 4:406–425. Stermitz, F. R., M. S. Abdel Kader, T. A. Foderaro, Schoonhoven, L. M., T. Jermy, and J. J. A. van Loon. and M. Pomeroy. 1994. Iridoid glycosides from 1998. Insect-Plant Biology: From Physiology to some butterflies and their larval food plants. 26 The ecology and evolution of melitaeine butterflies

Phytochemistry 37:997–999. Euphydryas maturna (Nymphalidae: Melitaeini) Stermitz, F. R., G. N. Belofsky, D. Ng, and M. C. in Finland. Nota lepidopterologica 21:154–169. Singer. 1989. Quinolizidine alkaloids obtained by Wahlberg, N. 1999. The habitat of Euphydryas Pedicularis semibarbata (Scrophulariaceae) from maturna in Finland. [In Finnish with English sum- Lupinus fulcratus (Leguminosae) fail to influence mary]. Baptria 24:173–177. the specialist herbivore Euphydryas editha Wanntorp, H.-E., D. R. Brooks, T. Nilsson, S. Nylin, (Lepidoptera). Journal of Chemical Ecology F. Ronquist, S. C. Stearns, and N. Wedell. 1990. 15:2521–2530. Phylogenetic approaches in ecology. Oikos Stermitz, F. S., D. R. Gardner, F. J. Odendaal, and P.R. 57:119–132. Ehrlich. 1986. Euphydryas anicia (Lepidoptera: Warren, M. S. 1987. The ecology and conservation of Nymphalidae) utilization of iridoid glycosides the butterfly, Mellicta athalia. II. from Castilleja and Besseya (Scrophulariaceae) Adult population structure and mobility. Journal host plants. Journal of Chemical Ecology of Applied Ecology 24:483–498. 12:1459–1468. Warren, M. S. 1991. The successful conservation of Strong, D. R., J. H. Lawton, and T. R. E. Southwood. an endangered species, the heath fritillary butter- 1984. Insects on Plants: Community Patterns and fly Mellicta athalia, in Britain (UK). Biological Mechanisms. Harvard University Press, Cam- Conservation 55:37–56. bridge, MA. Warren, M. S. 1992. Butterfly populations. Pp. 73–92 Thomas, C. D., and I. Hanski. 1997. Butterfly meta- in R. L. H. Dennis, ed. The Ecology of Butterflies populations. Pp. 359–386 in I. A. Hanski and M. in Britain. Oxford University Press, Oxford. E. Gilpin, eds. Metapopulation Biology: Ecology, Warren, M. S. 1994. The UK status and suspected Genetics, and Evolution. Academic Press, San metapopulation structure of a threatened Euro- Diego, CA. pean butterfly, the marsh fritillary Eurodryas Thomas, C. D., D. Jordano, O. T. Lewis, J. K. Hill, O. aurinia. Biological Conservation 67:239–249. L. Sutcliffe, and J. A. Thomas. 1998. Butterfly Vawter, A. T., and P.F. Brussard. 1975. Genetic stabil- distribution patterns, processes and conservation. ity of populations of Phyciodes tharos (Nympha- Pp. 107–138 in G.M. Mace, A. Balmford and J. R. lidae: Melitaeinae). Journal of the Lepidopterists’ Ginsberg, eds. Conservation in a Changing World. Society 29:15–23. Cambridge University Press, Cambridge. White, R. R. 1980. Inter-peak dispersal in alpine Thomas, C. D., and M. C. Singer. 1987. Variation in checkerspot butterflies (Nymphalidae). Journal of host preference affects movement patterns within the Lepidopterists’ Society 34:353–362. a butterfly population. Ecology 68:1262–1267. White, R. R., and M. P. Levin. 1981. Temporal varia- Thomas, C. D., and M. C. Singer. 1998. Scale-depend- tion in vagility: Implications for evolutionary ent evolution of specialization in a checkerspot studies. American Midland Naturalist 105:348– butterfly: from individuals to metapopulations 357. and ecotypes. Pp. 343–374 in S. Mopper and S. Y. White, R. R., and M. C. Singer. 1974. Geographical Strauss, eds. Genetic Structure and Local Adapta- distribution of host plant choice in Euphydryas tion in Natural Insect Populations. Chapman & editha (Nymphalidae). Journal of the Lepidopter- Hall, New York, NY. ists’ Society 28:103–107. Thomas, C. D., M. C. Singer, and D. A. Boughton. Williams, E. H. 1988. Habitat and range of 1996. Catastrophic extinction of population Euphydryas gillettii (Nymphalidae). Journal of sources in a butterfly metapopulation. American the Lepidopterists’ Society 42:37–45. Naturalist 148:957–975. Vogel, K. 1996. Zur Verbeitung, Populationsökologie Thomas, J. A. 1984. The conservation of butterflies in und Mobilität von Melitaea didyma (Esper, 1779) temperate countries: past efforts and lessons for im Raum Hammelburg, Unterfranken. Oedippus the future. Pp. 333–353 in R. I. Vane-Wright and P. 13:1–26. R. Ackery, eds. The Biology of Butterflies. Vogel, K., and J. Johannesen. 1996. Research on po- Princeton University Press, Princeton, New Jer- pulation viability of Melitaea didyma (Esper, sey. 1779) (Lepidoptera, Nymphalidae). Pp. 262–267 Thomas, J. A. 1993. Holocene climate changes and in J. Settele, C. Margules, P. Poschold and K. warm man-made refugia may explain why a sixth Henle, eds. Species Survival in Fragmented Land- of British butterflies possess unnatural early- scapes. Kluwer Academic Publishers, Dordrecht. successional habitats. Ecography 16:278–284. Zimmermann, M., N. Wahlberg, and H. Descimon. Wahlberg, N. 1997. The life history and ecology of 2000. Phylogeny of Euphydryas checkerspot but- Melitaea diamina (Nymphalidae) in Finland. terflies (Lepidoptera: Nymphalidae) based on mi- Nota lepidopterologica 20:70–81. tochondrial DNA sequence data. Annals of the Wahlberg, N. 1998. The life history and ecology of Entomological Society of America 93:347–355.