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Butterflies and Plants: a Phylogenetic Study

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Etoluriotr.52(2).1 991{p. p. .113560 2 BUTTERFLIES AND PLANTS: A PHYLOGENETIC STUDY Nrxl,qs J,qNzrR Nn SOnENN yr-rN Departntenrt tf Zoologt',U nit,ersityo J Stockholn,1 06 91 StockholmS, wedert IE -ntail : niklas.jan z.@z .oolog i. su.s e Abstract.-A database on host plant records frorn 437 ingroup taxa has been used to test a number of hypotheses on the interaction between butterflies and their host plants using phylogenetic methods (sirnple character optinrization. concentrated changes test, and independent contrasts test). The butterfly phylogeny was assembled from various s()urces irnd host plant clades were identified according to Chase et al.'s rbcJ--basedp hylogeny. The ancestral host plant appears to be associated within a highly derived rosid clade, including the family Fabaceae. As fossil data suggest that this clade is older than the butterflies, they must have colonized already diversilied plants. Previous studies also suggest that the patterns of association in most insect-plant interirctions are more shaped by host shifts, through colonization and specialization. than by cospeciation. Consequently, we have focused explicitly on the mechanisms behind host shilis. Our results confirm, in the light of new phylogenetic evidence, the pattern reported by Ehrlich and Raven that related butterflies feed on related plants. We show that host shifts have generally been rnore comrnon between closely related plants than between nore distantly related plants. This finding. together with the possibility ofa highertendency of recolonizing ancestral hosts, helps to explain the apparent large-scale conservation in the patterns of association between insects and their host plants, patterns which at the same tinle are more flexible on a more detailed level. Plant growth form '*'as an even more conservative aspect of the interaction between butterflies and their host plants than plant phylogeny. However, this is largely explained by a higher probability of colonizations and host shifts while 1'eedingo n trees than on other growth fonns. Ke\, words.-Coevolution, host shifts, insect-host plant interactions, Lepidoptera. Papilionoidea. specialization. Received March 22, 1996. Accepted November 2.6, 1991 Few systems have played such an important role in our butterfly fossil dates back to 48 M.Y.B.P and the diversifi- understanding of how species interactions evolve as butter- cation of the butterfly families probably took place at the end flies and their host plants. To a large extent this is the result of the Cretaceous,a bout 66 M.Y.B.P (Emmel et al. 1992). of a single influential paper by Ehrlich and Raven (196.1). At least some families even in the most recently derived of Their essay inspired a flood of paperi on difl'erent aspectso f the plant clades used in this analysis date to this time, such this association, and a number of related hypotheses on the as, Urticaceae( a member of Rosid I in Chase et al., 1993): evolution of insect-plant interactions have emerged. How- 90 M.Y.B.P.,R utaceae( Rosid 2): 52 M.Y.B.P.,A piaceae( As- ever, there have been few attempts to exploit the large da- terid 2): 52 M.Y.B.P., Apocynaceae( Asterid l): 60 M.Y.B.P. tabase on butterfly-host plant affiliations to test such hy- (dates fiom Eriksson and Bremer 1992). Therefore, the clades potheses using phylogenetic methods (Mitter and Brooks themselves must be even older. It is reasonable to regard the 1983; Miller 1987a). A major reason for this is that well- evolution ofcurrent associationsa s arising generallyt hrough supported phylogenies. fbr both butterflies and seed plants, butterfly colonization of already-diversified hosts, and that have been unavailable.H owever, this is slowly changing,a nd is the approach we shall take. This is not to say that coevo- today it is possible to put together reasonably robust phy- lution is an unimportant process in the interaction between logenies for both groups. Chase et al. (1993) have recently butterflies and their host plants. only that evidence fbr it published a molecular phylogeny for all seed plants, which should be sought at other levels of resolution. is probably the best estimate of large-scale angiosperm phy- There are two fundamentally different approachest o com- logeny to date. Butterfly phylogenies are also emerging and parative analyses using phylogenetic data. One approach we have constructed a plausible phylogeny across the but- seeks to find and explain general ecological or evolutionary terflies by combining these published estimates. correlations( Felsenstein1 985; Grafen 1989; Harvey and Pa- Ehrlich and Raven ( I 964) argued that the patterns of host gel 1991: Pagel 1992), while the other seekst o reconstruct plant association that we observe today have been shaped by and explain particularh istoricale ventso r sequenceso f events a stepwise coevolutionary process in which plants evolve along branches in a phylogeny (Mitter and Brooks 1983: defensesa gainst natural enemies,a nd these enemies in turn Coddington l98U; Sill6n-Tullberg 1988; Maddison 1990, evolve new capacitiest o cope with thesed efenses.P lantst hat Brooks and Mclennan l99l). These approachesa re com- escapef iom herbivores can diversify in the absenceo l'en- plernentary (Coddington 1994; Nylin and Wedell 199,1;P agel emies.I nsectst hat eventually managet o colonize one ol'these 1994) and we have in the presentp aper used both, depending plants will enter a new adaptivez one and can in turn diversify on the prcblem. onto the relatives ol' this plant, becauset hey will be chem- The question of ancestral host associationsi s a clearly ically similar. Ehrlich and Raven argued that thesep rocesses historical problem. On what plant did the first butterfly feed'/ have led to the main pattern they had observed,n amely that This question is interesting in its own right, but answering related butterflies tend to f'eed on related groups of plants. it also provides necessary information for any phylogenetic Most or all plant diversificatir)nu p to the level of resolution tests regarding direction of evolution of host plant associa- used in our analysis had probribly already taken place at the tions. Ehrlich and Raven (1964) regardedi t most likely that time the butterflies started to diversify. The oldest known the ancestral host plant family was Aristolochiaceae. ln con- 486 1 - il 9 9 l J T h c -S o c i c t l ,l i r r t h c S t r " r dov l ' E , r o l u t i o n .A l l r i g h t s r c s c r v c d B U T T E R F L I E S A N D P L A N T S 487 trast, Scott (1986) noted that Fabaceae were eaten by the Are patternso f butterflyh ost plant utilizationn onrandoms o most basal branches of several butterfly families and sug- that relatedb utterfliesf eed on relatedp lants,a s suggestedb y gested that the ancestral host probably was a legume. More Ehrlich and Raven?( 2) What was the ancestralh ost plant recently, Ackery (1991) suggestedt hat Malvales may instead associationa, nd has this associationc onstrainedh ost plant be lhe anceslralh ost association. utilizationi n butterflies?(3 ) Are hosts hiftsi nvolving closely Ehrlich and Raven (1964) noted several factors influencing relatedp lant speciesm ore common than shifts to more dis- the association between butterflies and their host plants, but tantly related plants'?( 4) Are there idenrifiableg roups of particularly stressedt he importance of the plant's secondary unrelatedp lants that often occur togethera s hosts?( 5) Is metabolic substances.T hey noted that many higher taxa of plant phylogenya morec onservativea specto fbutterfly-plant plants are characterized by distinctive secondary chemistry, associationsth an plant growth fbrm, or vice versa?( 6) Are and cited a number of examples in which related butterflies major host shiftsm ore commoni n woody-plant-feedingth an feed on related plants. They also cited examples where related in herb-f'eedinglin eages?( 7) Are tree-feedingb utterflyt axa butterflies are t'eeding on unrelated plants with chemical sim- associatedw ith a largern umbero f host plant cladest han are ilarities. These observations are consistent with, though not herb-feedingt axa? sufficient to demonstrate, the importance of plant chemistry. However, nobody has tried to determine whether and at what MErnoos taxonomic scales the tendency to feed on related plants is Unlesso therwises tated,a ll analysesh aveb eenc arriedo ut statistically demonstrable for butterflies as a whole, as op- usingt hec omputerp rogramM acClade( vers. posed to selected examples. 3.05,M addison and Maddison 1992). Although plant chemistry has been viewed as the prime factor governing the evolution of butterfly-host plant asso- Phylogenies ciations (e.g. Feeny 1915, 1976, l99l; Jermy 1916, 1984 Scriber and Slansky 1981: Berenbaum 1983; Zangerl and The plant phylogenyu sedi n this study follows the rbcl- Berenbaum 1993; Fiedler 1995b), other aspects of the host, baseda nalysiso f seed plant relationshipsb y Chase et al. not necessarily well correlated with phylogeny, might also (1993).T hey perfbrmedt wo diff'erents earchesu sings lightly have a large eff'ect (Benson et al. 1975; Smiley 1978; Price different taxon sampling and weighting procedures.T hese et al. 1980; Courtney 1984; Bernays and Graham 1988; An- searchesp roducedv ery similart rees.W e havef br the present derson 1993). One example is host growth form. Different analysisu sedt he treep roducedb y their search2 (or treeB ), growth forms can dominate in different habitat types, which which they judged to be the most reliable.C hasee t al. sum- have distinct combinations of microclimate, enemies, etc.
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