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http://www.jstor.org OIKOS57: 119-132. Copenhagen1990

Minireviewsprovides an opportunityto summarizeexisting knowledge of selected MINI- ecologicalareas, with specialemphasis on currenttopics where rapidand significant advancesare occurring.Reviews should be concise and not too wide-ranging.All key REVIEW referencesshould be cited. A summaryis required.

Phylogenetic approaches in ecology

Hans-Erik Wanntorp, Daniel R. Brooks, Thomas Nilsson, Soren Nylin, Fredrik Ronquist, Stephen C. Stearns and Nina Wedell

Wanntorp,H.-E., Brooks, D. R., Nilsson,T., Nylin, S., Ronquist,F., Stearns,S. C. and Wedell, N. 1990. Phylogeneticapproaches in ecology. - Oikos 57: 119-132.

This paperargues that manyecological studies could benefit greatly from a phylogen- etic approach.For this purpose, cladisticsis an appropriatemethod to reconstruct phylogeny.Case studies from seven researchtopics in ecology are reviewed. In all studies, historicalexplanations have played a centralrole, and mostly, cladograms have been used. Connectionsto statisticalmethods for estimatingquantitative vari- ation amongtaxa are discussed.A phylogeneticbase would greatlystrengthen both problemformulation and analysis.This is true for populationstudies as well as for all areas where adaptationalexplanations are invoked;single species studies as well as comparativestudies or coevolution studies. Three cladistic proceduresuseful in ecologicalresearch are brieflydescribed. Ecology and systematicshave much to offer each other and it is a challengeto bringthe two fields together.

H.-E. Wanntorp and T. Nilsson, Dept of Botany, Univ. of Stockholm, S-10691 Stockholm, Sweden. - D. R. Brooks, Dept of Zoology, Univ. of Toronto, Toronto, - Ontario, Canada M5S 1A1. S. Nylin and N. Wedell, Dept of Zoology, Univ. of Stockholm, S-10691 Stockholm, Sweden. - F Ronquist, Dept of Zoology, Uppsala Univ., Box 561, S-75122 Uppsala, Sweden. - S. C. Stearns, Dept of Zoology, Univ. Basel, Rheinsprung 9, CH-4051 Basel, Switzerland.

But a still more important consideration is that the chief part of the organisation of every living creature is due to inheritance; and consequently, though each being assuredly is well fitted for its place in nature, many structures have now no very close and direct relations to present habits of life. (Darwin 1859)

Introduction more quickly than would be possible with a single hy- pothesis (Chamberlain 1897). In 1897, William Chamberlain, the President of the Ecology and population biology have been dom- American Society of Geologists, spoke convincingly on inated by explanations rooted in processes observable the role of alternative explanation in science. By help- today. Evolution has often been seen as rapidly bringing ing one to resist the temptation to confirm one's favou- populations into equilibrium with local conditions, an rite hypothesis, the comparison of alternative explana- equilibrium in which the existence of certain genotypes tions maintains objectivity, demonstrates error earlier and phenotypes is explained through their having been in an investigation, and leads one closer to the truth the best available. In community ecology, the historical

Accepted 13 September1989 © OIKOS

OIKOS 57:1 (1990) 119 0 A B siomorphies) are identified by using outgroup compari- son - any trait found in at least one member of the group being studied that is also found in species outside the group is most parsimoniously interpreted to have evolved prior to the origin of the common ancestor of the group, and is hence plesiomorphic. The correspond- la ing traits not present in the outgroup are then relatively derived (apomorphies). Once a collection of apomor- phies has been assembled for a group, cladistic analysis groups the species according to their shared apomor- phies (synapomorphies) (Fig. 1). Due to parallel and convergent evolution, not all apomorphies will conform to a single pattern, however. Contemporary cladistics Fig. 1. Cladogramof three species, A, B and C. The traitslb, uses a variety of numerical methods and computer- 2b, 3b and 4b are interpretedas primitivebecause they occur assisted programs for discerning the pattern of syn- also in the outgroup,0. la and 2a are commonspecializations apomorphies that best fits the data at hand (Wiley 1981, B a in C. unitingspecies and C. 3a is uniquespecialization Trait Fink 1986, Platnick 1989). The pattern that results is a 4a is homoplasticand has arisenindependently in A and C as a convergence. hypothesis of cladistic relationship, a cladogram, which can be interpreted as a phylogenetic tree to support historical explanations in biology. Cladograms are atemporal representations of relationship. They say approach to hypothesis formation has been, until re- nothing about the process of evolution. In contrast, cently, equally negligible. Only in the biogeographical phylogenetic trees are historical interpretations of cla- and geobotanical traditions has historical explanation dograms. The relationship represented in one clado- continued to play a central role. gram is compatible with more than one phylogeny (Nel- While ecology has been maturing as an experimental son and Platnick 1981). Wiley (1981) is a useful hand- and theoretical science, cladistics has increased the rigor book for those further interested in cladistic analysis. of historical explanations. This rigor has made the ex- Cladistics is, thus, a method that uses traits to in- planations based on phylogenies more reliable and vestigate the systematic relationship of organisms. more testable than they had previously been. At the Comparative biology, on the other hand, uses clado- same time, their own results have led ecologists to re- grams to investigate the systematic or temporal distribu- evaluate the role of adaptation, and they have begun to tion of traits. The idea of using the comparative ap- analyze comparative data with the aim of identifying proach to historical explanations in ecology was wide- historical constraints. spread in the 19th century and has continued as a Community ecology and evolutionary ecology have central theme in the European geobotanical tradition been suffused with experimental and theoretical ap- and in comparative morphology (Riedl 1978, Lauder proaches in the last quarter century, and some of them 1982). It has become increasingly prominent in ecology. have been making rapid progress on adaptationist as- The historical approach complements the current adap- sumptions. Because this progress has uncovered some tationist approach to evolutionary ecology. The main patterns not readily explained by adaptation, attention difference is the use of indirect estimates of history and has turned to techniques that can partition the effects of the emphasis on adaptation in evolutionary ecology and adaptation and constraint (reviewed by Pagel and Har- the use of direct estimates of history (through phyloge- vey 1988). netic trees) and the emphasis on constraint in historical The use of cladistics in comparative biology has be- ecology. Historical ecology is best suited to asking ques- come more widespread only during the last few years. tions about the origins and diversification of ecological Cladistics is a method of analysis, also known as phylo- phenomena, ranging from life history traits to commu- genetic systematics, that was first developed by the Ger- nity structure. As a form of comparative biology, it is a man entomologist Willi Hennig (Hennig 1950, 1966). method for suggesting patterns and locating possible Hennig devised it as an empirical method for discov- adaptations. It is a method for discovery and descriptive ering and justifying phylogenetic relationship. All spe- explanation but it can also, indirectly, discriminate cies are mosaics of primitive and derived traits, and the among causal explanations (O'Hara 1988), e.g. through phylogenetic relationships in a group of species can be statements about the sequence of origination of traits. deduced from the pattern of their shared derived traits. This paper reviews case studies in which a historical The method is thus based on (1) determining which approach has produced alternative explanations that traits are relatively primitive and which are relatively have brought insight into ecological problems. The case derived with respect to the group being studied and (2) studies illustrate methods and suggest connections to grouping the various species according to their shared other quantitative techniques, such as nested analysis of derived traits. The relatively primitive traits (called ple- variance developed below. Wider use of historical ex-

120 OIKOS 57:1 (1990) Examples of the phylogenetic approach c '0.< ' - Leaf retentionin oaks c ^ Identifyingadaptations The European oak is well known for its habit of retain- its leaves far into the winter. This is no- CZ ing especially .u~~. ticeable in young specimens and makes them conspi- E 0 EE4) E cuous in the deciduous woodland they inhabit. Several stories have been proposed to explain leaf retention as an adaptation (e.g., Otto and Nilsson 1981, Nilsson 1983). Wanntorp (1983) showed how cladistic methodology can be used to identify traits as candidates for actualistic adaptive explanation and to rule out non-candidates: In broad perspective, temperate deciduous woodlands can be seen as an extreme habitat for oaks. Most of the hundreds of oak species inhabit regions with Mediterra- nean or tropical climates. All oaks of warmer climates are evergreen, and close relatives of the European oak are semi-evergreen (Fig. 2). Leaf retention is ancestral Quercussect. in oaks and needs no special explanation in European Lepidobalanus oak. Among recent oaks, deciduousness is the derived beeches oaks condition that needs an adaptational explanation. Most traits in any organism are ancestral, a legacy of its history. The inheritance of the trait from ancestors should always be considered as the evolutionary null- hypothesis. Only the traits, demonstrated to be novel in the phylogeny - the autapomorphies - should be chosen 2. of oaks that Fig. Simplified cladogram showing evergreen- as candidates for explanations that invoke actual envi- ness is an ancestral trait within the genus Quercus. In Eu- ropean oak and some other species, deciduousness has evolved ronmental conditions. as a specialization to cold climates. Wanntorp concluded: "Already when formulating theories on which the traits are that one might investi- gate, one should have at least some idea about relation- ship. Otherwise one might, as in the oak example, dis- planation in ecology would enrich ecology and lead cuss the vestigial ancestral condition (leaf retention) phylogenetic systematics into constructive engagement when the opposite (deciduousness) is the specialization with a field in which it has much to offer. in the actual species." For the sake of argument, we will take an adapta- A similar approach was applied to the origin of the tionist approach throughout this paper, accepting that orb web in spiders by Coddington (1986). Intricate orb whenever a new trait arises, it does so as the result of webs were traditionally thought to be a convergent natural selection. We will consider phylogeny and his- adaptation, derived in different spider groups from cob tory, not as providing alternatives to adaptation, but as web types. Coddington, however, demonstrated orb a means of ordering the adaptationist explanations. The webs to be an ancestral trait for a large group of spiders discussion whether specific traits should be interpreted and the "simpler" cob webs to be derived from this as adaptations at all, falls without the scope of this condition. Like in the oak example, the sequence is review. reversed, and with it the neeed for adaptive explana- We will adhere rigorously to the principle of parsi- tion. The orb web is still a candidate for adaptive expla- mony - not because the concept of parsimony is applica- nation, but at a much more general level. Like in the ble to evolution or any process of nature, but because it oak example, the strength of the phylogenetic approach is a necessary tool in our attempts at explaining those is evident already at the level of problem formulation. processes. Thus, change always requires an explana- There are few examples in the literature, but Greene tion, while inertia does not. To explain absence of (1986) fruitfully used this approach for identifying and change a priori as evidence that some agent (such as studying possible adaptations in monitor lizards (Vara- natural selection) is at work would indeed be an un- nidae). necessary multiplication of theories. Behaviouralecology - Sex in sticklebacks Sticklebacks and their relatives (Family Gasterosteidae) have played a leading role in behavioural and ecological

OIKOS 57:1 (1990) 121 Fig. 3. Cladogramof sticklebacks 40 / (Gasterosteidae)based on /p" / /·3 / / behaviouraland nest- buildingtraits.

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research for decades. One dominant paradigm in beha- 1982). The idea was straightforward: the first mutants vioural ecology asserts a tight connection between indi- with warning coloration would be eaten, or damaged vidual and social behaviour on the one hand, and envi- and killed, and only their siblings would benefit, for ronmental conditions on the other. Breeding systems, predators were thought to learn slowly and to kill their territorial defence, the opportunity for sexual selection, prey before determining their toxicity. Under this hy- and many other aspects of behavioural biology are seen pothesis, gregariousness had evolved first providing as resulting from selection imposed by actual conditions conditions in which aposematic coloration could then of the contemporary local environment. evolve through kin-selection. In this context, a phylogenetic analysis carried out on sticklebacks by McLennan et al. (1988) is particularly intriguing. They constructed a stickleback cladogram from strictly behavioural traits using the PHYSYS pro- .S_ gram (Mickevich and Farris 1982). Their tree based on E behavioural traits is closely concordant with trees based S = oY .o m o IQ on morphological traits and has an even higher consis- (£Q.0<(< CL Q_< UJLLiuJ-0 tency index, indicating a high overall level of historical constraint and a low degree of evolutionary plasticity '~Cl) 0. 0 0 - .j .~0 E.- Cl) : ) o .- 8'cE 3o o 0 30x Eo . for the behavioural traits used to construct the tree (Fig. ,:Lo X.-.~ 0 6X 0~ 0~ 0Q.o 0.W LL < = 3). .Dn* ~ This result, coupled with the observation that a num- ber of stickleback species are ecological generalists, ranging across a broad variety of environmental condi- tions and carrying the same behaviour patterns with them across that range, suggests that history and phylo- geny have played a larger role in the determination of patterns of behaviour in sticklebacks than has adapta- tion to the actual local environments. Again we see here a constructive phylogenetic alternative that strongly suggests the need for a reappraisal of earlier adapta- tionist hypotheses.

Orderof origin- Warningcoloration and gregariousnessin Fig. 4. Cladogram of some white butterflies (Pierinae). The butterflies occurrence of warning coloration (W) and gregariousness (G) are shown on The of these traits are shown as bars It has long been thought that the development of apose- top. origin on the cladogram. (Outgroup comparison shows that cryptic matic, or warning, coloration required the involvement and solitary larvae are ancestral.) In no case can gregariousness of kin selection (Fisher 1930, Turner 1971, Harvey et al. be demonstrated to arise before warning coloration.

122 OIKOS 57:1 (1990) IQ) 0 accumulating, and closer analysis of the logic leading to V_. ID the predictions demonstrated that there was no clear I foundation for the predicted association between K- § selection and the life-history traits. E fi E | : E H .H Stearns (1977) found that about half the species for E('3 g g g G W E E .5. § which the data are reliable - for intra-specific or intra- 4c- 'C-3) B generic comparison - fit, and about half did not. He i § ;0 later (Stearns 1980) suggested that our impression that A A A most species could be arrayed along a single dimension was not due to microevolutionary processes acting within species, but to comparisons arising at the level of F F F F F the family, the order, and the class. In an analysis of NX v w life-historyvariation in the mammals,based on multiva- riate statistics, Stearns (1983) found that most of the r pattern of covariance in life-history traits that we call /A- r&K-selection results from correlations with two fac- tors: body size and phylogenetic relationship. When the influence of those factors is removed and the residuals are examined, much less of the covariance in the traits is left to be explained by microevolution operating within species. Brown (1983), in his work on snails, and Dun- ham and Miles (1985), in their work on reptiles, reached similar conclusions. None of these authors had access to cladograms and Fig. 5. Cladogramof some membersof the daisyfamily (Aster- they were therefore forced to use existing classifications aceae). The occurrenceof two traitswithin spe< cies are shown in their studies. Pagel and Harvey (1988) provide a - life F - few-flowered The on top. (A annual cycle, capitula.) useful overview and of the and weak- originsof these traitsare shown as bars on the critique strengths nesses of several alternative methods of doing such analyses. Sillen-Tullberg (1988) tested this idea vvith a phylo- Telenius et al. (1989 and unpublished) analyzed the genetic analysis of butterflies. She used thie best avail- distributions of life history traits in eleven species of the able taxonomies, for in most cases cladograams were not plant family Asteraceae using a cladogram derived from available. Her focus was on the order off events: did a study of the tribe Anthemidae by Bremer and Hum- gregariousness evolve before, with, or after warning phries (in press) (Fig. 5). Three of the species were coloration? The test was decisive: in 15 cases gregari- annuals, together forming a monophyletic group. The ousness had evolved after warning colorati(on, and in no interpretation was that the annual life cycle evolved case had it evolved before warning colorat ion. In three once in the common ancestor of these species and does cases, the two traits could not be separateci, and in five not need special explanations in the three genera. On cases gregariousness had evolved in line.ages without the other hand, few-flowered capitula occurred in the warning coloration (Fig. 4). two distantly related genera Artemisia and Achillea, and The evidence presented by Sillen-TullIberg speaks was interpreted to have evolved independently within against the kin selection hypothesis for tthe origin of each genus. When relating the number of flowers to the warning coloration. Here phylogenetic aanalysis pro- type of pollinating agent, they found that few flowered vided a powerful test that falsified a spe cific kind of capitula were correlated with a generalist pollinating adaptational explanation and supports a

OIKOS 57:1 (1990) 123 (AB) (AB) (ABC) (ABCD) the fitness of their host plants. Therefore, plants which A B C D a b c d by chance acquire traits (defence mechanisms) that make them unpalatable to phytophagous insects will increase their fitness, and the new defence mechanism will spread throughout the plant species. In the absence of phytophagous insects the plant lineage will then rap- idly radiate. However, sooner or later some individual a. Host plant phylogeny b. Allopatric co-speciation insects will overcome the new defence mechanism and be able to feed on the previously protected plant group. These individuals will increase their fitness because they (A) (B) (C) (D) (D) (C) (B) (A) a b c d a b c d will avoid competition from other phytophagous in- sects. Therefore, the ability to overcome the new de- fence mechanism will spread throughout the species. In the absence of competitors, the insect lineage will di- versify to exploit the previously protected plant group. Exactly as the allopatric co-speciation model, the exclu- sion model a non-random between c. Exclusion model d. Colonization model predicts congruence insect and plant However, ac- Fig. 6. Differentmodels for the evolutionof insect-hostplant phylogenies (Fig. 6c). associationsand examplesof the type of fit betweeninsect and cording to the exclusion model, the co-speciation events plant phylogeniesthey predict.All species are assumedto be will be found to be sympatric (rather than allopatric) sympatric.This means that the allopatricco-speciation model and not associated with persistent vicariance patterns. is the extreme case where all have representedby species Furthermore, events will tend to be asso- secondarilybecome sympatric.Lower case letters refer to in- co-speciation sect species and uppercase letters to plant species. Lettersin ciated with specialization in the insect, i.e., narrowing bracketsrefer to host plant recordsof insect species. rather than broadening of the host plant range of the insects. We should expect some insect lineages to spe- cialize on single host plant clades because the insects between insect and plant phylogenies, and thus can be have overcome the defence system of the plants; we tested using phylogenetic methods (Mitter and Brooks should expect other insect lineages to be excluded from 1983, Miller 1987). certain host plant clades because the insects have not To exemplify this approach, we briefly discuss three overcome the defence systems of the plants (when in- models for the evolution of insect-host plant associ- sect phylogenies are mapped on host plant phylogenies ations and the type of fit between insect and host plant it is sometimes possible to detect such exclusion events phylogenies they predict (cf. Fig. 6). We also cite a few because they appear as extinctions of insect lineages; case studies supporting two of the models. see Brooks 1988).

Colonization model (Jermy 1976, 1984) Allopatric co-speciation (Brooks 1979) According to this model, diversification of phytopha- In this model, congruence between insect and host plant gous insects took place after the radiation of the host phylogenies is expected because of simultaneous allo- plants and was independent of plant speciation. The patric speciation in insect and host plant lineages, i.e., insects colonized new host plants numerous times dur- vicariance events. We expect some of these co-specia- ing their evolution. If this model is correct, we expect tion events to persist as concordant insect and host plant little or no congruence between insect and plant phylo- vicariance patterns. Because in this model co-speciation genies (Fig. 6d). A special type of the colonization is independent of any changes in host preference or host model was proposed by Ehrlich and Raven (1964), who suitability, there are no general predictions about suggested that host shifts occur predominantly between changes in the host plant range of the insects that can be plants with similar secondary metabolites. attached to it. However, when sympatry between lin- eages is established subsequent to a co-speciation event, Two examples - gall midges and butterflies we may expect a tendency towards broadening of the Only few studies using a phylogenetic approach to ex- host plant range of the insects (Fig. 6b). Until lately, amine the evolution of insect-host plant associations this model has received very little attention in the litera- have been published so far. Roskam (1983, 1985) used ture on insect-host plant associations. cladograms to investigate the evolution of the associ- ation between Semudobia gall midges and their host plants, birches (Betula spp.). The cladograms are highly Exclusion model (Ehrlich and Raven 1964, Berenbaum congruent, because all four speciation events in the 1983) Semudobia cladogram correspond with dichotomies in This is the "classical" coevolution model and may be the Betula cladogram (no. 1-4 in Fig. 7). Of the two summarized as follows. Phytophagous insects reduce descendant species after the first speciation event in the

124 OIKOS 57:1 (1990) Semudobia skuhravae 1. Costatae 4 Heliconiusbutterflies (Mitter and Brooks 1983). We are (1,2,4,-11) 2. Humiles i not awareof any studiesto date that supportthe exclu- betulae 3. Acuminatae sion model. (6L710.11) 4. populifolia E It is importantto recognizethat even if colonization of new host plants is frequent, important aspects of brevipalpis 5. coeruleagroup (4,8) insect-host still be 6 platyphyllos plant relationshipsmay historically constrained.For instance,Nylin (1988) showed that the 7 pendula I polyphagous nymphalid butterfly Polygonia c-album steenisi 8 papyrifera (519) displays a distinct preference for hosts in the order 9 fontinalis Urticales,and larvaealso grow fasteron these hosts. A 10 davurica preliminaryphylogenetic analysis (Nylin, unpubl.) re- \ tarda 11 pubescens w PAL (10,11.6,7) veals that the polyphagousgenera Polygoniaand Nym- evolved from an ancestor on Urtica- Fig. 7. Evolution of the association between birches, Betula phalis specialized spp. andgall midges,Semudobia spp. Numberednodes refer to ceae. Thus, despite the colonizationof manynew hosts, co-speciation events; numbers in parentheses refer to host the ancestral ties with Urticales persist in Polygonia plants of gall midges (main host underlined). HOL = Holarc- c-album. = tic, PAL Palaearctic, NA = Neartic region; E = East, W = Insect-host associationsconstitute one ex- West; Pub. = Sect. Pubescentes, Verr. = Sect. Verrucosae. plant only From Roskam (1985). ampleof coevolvingspecies associationsfor whichphy- logenetic methods promise to give new insights. The majority of phylogenetic studies in coevolution pub- lished to date have been based on helminthand arthro- gall midges, one (S. skuhravae) retains a broad host pod parasites of vertebrates (see Brooks 1988 for a range and now induces galls in bracts of fruit catkins of review). The possible coevolutionbetween other inter- birches belonging to all sections of Betula except Acu- acting components of ecosystems, such as predator- minatae, which hosts no gall midges. The other, the prey or pollinator- plant associations,has been little stem species of the remaining Semudobia species, is discussedin phylogeneticterms. The most useful meth- specialized on birches belonging to the section Excel- ods for comparingphylogenies of putativelycoevolving sae. The narrow host range of the latter species is ex- groups, consensus trees and parsimonymapping, are plained by the exploitation of a new resource, decid- reviewedbelow. uous fruits, a derived condition only present in birches belonging to the sections Excelsae and Acuminatae. Communityecology - Regionalexplanations of local After the second speciation event in the gall midges diversity there is only weak specialization in the descendant lin- Ricklefs (1987) argues convincingly that community eages (Roskam and van Uffelen 1981), leading to a ecology has relied mostly on local-processtheories in "doubling" of the host plant records of the remaining explanationsof patternsstrongly influenced by regional Semudobia species. The third and fourth co-speciation processes.Local explanationsrely on the actionof com- events are vicariance events, for there is a correspond- petition, predation and disease to explain patterns of ing pattern of allopatric speciation in Semudobia and species diversityin small areas, from hectaresto square Betula. Even if there is one possible exclusion event, kilometres.The communityis seen as maintainedin a which could indicate the evolution of a novel defence saturatedequilibrium by biotic interactions. mechanism in birches belonging to the section Acumi- However, independentlines of evidence suggestthat natae, the overall pattern in Semudobia and Betula is regional diversity plays a strong role. That there are clearly best fit by the allopatric co-speciation model. four to five times more mangrovespecies in Malaysia Host plant relationships in the butterfly family Papi- than in Costa Rica and four time more chapparalplant lionidae were considered strong evidence for the exclu- species in Israel than in California,that the numberof sion model by Berenbaum (1983). Miller (1987) com- cynipinewasps on a species of Californiaoak is strongly pared cladograms of butterflies in this family with tradi- related to the total numberof cynipinesrecorded from tional classifications of their host plants. He found very the whole range of the oak species, that local species little congruence between insect phylogeny and plant richnessin Caribbeanbirds is stronglyrelated to total classification. Thus, the evolution of papilionid host regional bird diversity, are all observationsthat one plant associations is characterized by numerous host cannot explain on the assumptionof local, saturated plant shifts. Furthermore, these shifts tend to occur equilibria- otherwisesimilar states would be attainedin between plants with similar secondary metabolites, thus systems experiencingsimilar conditions. The explana- supporting the colonization model of Ehrlich and Raven tion of local community structure in these systems (1964) but not the exclusionmodel. Patternssupporting shouldinclude historical and biogeographicinformation the colonizationmodel (not necessarilythe Ehrlichand - from cladisticsand biogeography. Raven variant)have also been reportedin the tephritid The communities of helminth parasites inhabiting fly genus Rhagoletis(Berlocher and Bush 1982) and in SouthAmerican freshwater stingrays provides a striking

OIKOS 57:1 (1990) 125 z z Radiations- are they adaptive? 0 0 0 N N z w The general definition of adaptive radiation is that an 0 0 -J z 0 ancestor colonizes a new adaptive zone, followed by 0 0 I z Tc CD radiation of descendant lines occupying the many empty w 3 niches. There are several examples of adaptive radi- 0 ations in the literature, however, few were examined from a phylogenetic stand-point. Brooks et al. (1985) studied how much of the diversi- fication among the families of digenetic trematodes (a group of parasitic flatworms) could be explained by adaptive changes in life history traits. They picked out traits assumed to have adaptive value, e.g., host type. They pointed out: "the ecological factors we used... are the same ecological factors that have been used to sup- port adaptationist explanations of digenean evolution". A cladogram, based on morphological characters (Brooks et al. 1985), was used to map the "adaptive" traits on. They discovered that only one fourth of the branch points, i.e., speciation events, were accompa- nied by changes in any of the "adaptive" traits. Fig. 8. Area cladogramof the riversystems in SouthAmerica, As a result of such findings, several classical cases of based on the and distributionof relationships sting ray para- radiation should be to cladistic sites (Brooks 1985). The Paranaseparated first, then the East adaptive subjected Amazon, the West Amazon, the Orinoco, and last the Mara- analysis in which the putative adaptations and the puta- caibo and Magdalenariver systems. tive environmental conditions with which they should be associated are introduced on the cladogram. Until such analyses show to what extent adaptations are asso- ciated with radiations, the word "adaptive" should be example. Brooks (1985) showed that the degree of his- dropped from the catch phrase "adaptive radiation". torical influence on helminth community diversity dif- The related subject of adaptive zones has seen the fered among six river areas in South America. The beginning of a cladistic treatment. Mitter et al. (1988) Parana system, the western Amazon, the Orinoco and tested the common suggestion that insect lineages which the Magdalena systems all contain species whose phylo- evolved phytophagy entered new adaptive zones and genetic relationships correspond to the geological his- were able to diversify as a result of overcoming this tory of the areas in which they occur (Fig. 8). The major obstacle in evolution. They showed that phy- Orinoco community also has many species that colon- tophagous clades of insects are consistently more spe- ized from other river systems. Therefore, it has the cies-rich than their non-phytophagous sister clades, thus highest diversity although it is not the oldest. In two supporting the notion that entering a new adaptive zone other areas, the Maracaibo basis and the eastern Ama- is followed by subsequent radiation. zon, the helminth communities also appear to have been partly derived from colonization events. The Ma- Combining cladograms with statistical analysis racaibo community has representatives from three dif- ferent source areas (the Magdalena, Orinoco and west- In this section we will discuss the possibility of combin- ern Amazon), while the eastern Amazon has repre- ing cladistics with statistical methods, i.e., analyses of sentatives from only a single source area (the Parana). variance, covariance and correlation. Such methods are The historical assembly of these communities has dif- widely used by ecologists, for the simple reason that fered among the river systems. The community of the most traits studied are quantitative and show consid- Parana system has almost entirely evolved locally, while erable variation. In contrast, cladistics and other sys- that of the Orinoco has a large colonist component. tematic methods prefer qualitative traits with little vari- Equilibrium explanations may be relevant for the latter, ation within taxa. By combining the two approaches it but absolutely not for the former system, where instead might be possible to find answers to some basic ques- an historical explanation is required. Again, the cladis- tions in ecology. For instance: one Great Tit laid eight tic approach shows its strength already in suggesting the eggs this year. The reason that it laid amniote eggs in appropriate framework in which the problems should be the first place goes back to the relationship between formulated. birds and dinosaurs and does not need a special expla- nation. But why eight eggs and not seven or nine? To what extent was this due to the Great Tit being a mem- ber of a certain order of birds, or suborder, superfamily,

126 OIKOS 57:1 (1990) 0 9- ent in a clade arises at higher taxonomic levels (e.g., ACebinae Brown 1983, Stearns 1983, Dunham and Miles 1985). 0-6- One explanation of this result, not well tested, is that ACallitrichidae variation is progressively delimited within clades by *Homo constraints peculiar to those clades. It would therefore 0-3- AAtelinae be of interest to study if the distribution of characters on RELATIVE AGE the cladogram suggests their involvement in constraints. AT MATURITY 0- AA Iouattinae To find out, one could construct a cladogram and in- [FEMALE] ALorisinae n A A., GalaginaeACercopithecinae Cheirogaledinae clude in it the evolutionary innovations for each clade -0-3- Altndriinae AColobinae thought to act as clade-specific constraints. These in- APongidae novations would be associated with deviations from mean values of the quantitative traits, e.g., life history -0-6 - Acallimico traits thought to be constrained in a clade-specific fash- _ .1 ion. These deviations could be calculated from a nested v -W v a - -1-, V v of variance or covariance. the -09 -0-6 -0-3 0 0-3 06 analysis By associating

RELATIVE NEONATAL WEIGHT evolutionary innovations hypothesized to be constraints Fig. 9. The relationshipbetween relative birth weight and with positive or negative residuals of the quantitative relativeadult weightin Primates.Relative measures were cal- trait for each clade, one could generate a hypothesis, culatedas deviationsfrom the line of best fit amongdifferent based on correlation, about a putative causal link be- subfamilies.The allometricrelationship does not arise among tween the evolutionary innovations and the quantitative species, but at higherlaxonomic levels (fromHarvey and Clut- ton-Brock1985). traits. At the same time, such information could be used to test alternative hypotheses about such links, for some hypotheses would be ruled out by the pattern observed. family (Paridae), genus (Parus) or species (P. major), and what part of the explanation belongs in the field of Phylogeniesand the comparativemethod population ecology or the study of environmental ef- fects and physiology? The answers to these questions New and refined methods aimed at finding answers to will vary depending on the species studied. For exam- questions like those outlined above are constantly arriv- ple, the whole bird order Procellariformes lays a single ing. The methods trace their roots to comparative ecol- egg, while clutch sizes vary considerably within the ogy. In recent years it has been realized that individual family Passerinae. species cannot be treated as independent data points in There are also related questions. Quantitative traits, analyses using the comparative method (Clutton-Brock studied by ecologists, are often interrelated in allomet- and Harvey 1977, 1979). This is because related species ric relationship or tradeoffs. Are the deviations from may share a character because of so called "phylogen- the ancestral state at each phylogenetic level coupled etic inertia" (i.e., constraints on development; e.g., with changes in associated traits (e.g., adult sizes with Clutton-Brock and Harvey 1979, Felsenstein 1985) or number of eggs) or with changes in life style (niche because, being similar species, they probably share shifts, feeding habits etc.)? many aspects of their ecological niches which may influ- Allometric relationships such as size-fecundity or ence the evolution of the trait under study (e.g., Ridley adult weight-birth weight vary within clades. Often, one 1983, 1989, Grafen 1989). Nested analysis of variance finds that most of the variation is not among species, but could be used to find the taxonomic level which contrib- among genera, sub-families or families (Harvey and utes the most to the variance in the studied trait, and Clutton-Brock 1985, Pagel and Harvey 1989). Within a then means can be compared for taxa at this level in- given species, such relationships function as the bound- stead of species means. Similar techniques were ary conditions on optimality problems in life-history adopted in several major comparative studies, such as evolution - as tradeoffs, and they have been used in Stearns' (1983) analysis of life history traits in mam- predictions of optimal life histories (e.g., Stearns and mals. Koella 1986). Such predictions can be surprisingly accu- The major drawback of this method is that phyloge- rate, and it would therefore be interesting to have a nies are used only to find the taxonomic level to study. method that would partition the prediction into compo- Means for higher taxa are not necessarily (or even prob- nents contributed, through the constraining allometric ably) independent (Felsenstein 1985, Bell 1989). Also, relationship by the family, sub-family, genus and so more or less equal variance may exist at several levels, forth. and (importantly if we are interested in studying how traits affect each other in evolution) covariance between traits be at levels other than the one where Tracingthe historyof constraints may greater variance in the dependent trait is greatest (Bell 1989). A number of studies have demonstrated that much of Harvey and coworkers (cf. Pagel and Harvey 1988) the variation and covariation of quantitative traits pres- have developed methods to get estimates of the con-

OIKOS 57:1 (1990) 127 Fig. 10. Inferring Used as Boundary Conditions in phylogeneticconstraint. - Inferred Phylogenetic Constraints Optimality Models to make Predictions Left. When plotted on a graph,the observedlife historydata for different species generatesa line for each subfamily.This line / Species the 6 represent phylogenetic x boundaryconditions at this / Subfamily (At taxonomiclevel. Estimates 400 of constraintsfor each 0 / ^^x Family subfamily,in turn, generate the boundaryconditions at the familylevel and so forth. - Right. The inferred constraintsare then used as boundaryconditions in Predicted optimalitymodels to predict Weight the optimallife history traits, or trade-offsbetween traits.The predictionsare plotted againstobserved values. In this graph,the distancebetween the points representsthe amountof changein the trait at each taxonomiclevel.

straining relationship at different taxonomic levels in a Even if two subfamilies are both monophyletic, they are given classification. Because many of the existing classi- directly comparable only if they are of equal age (e.g., fications are not based on cladistic principles, however, sister groups). A more direct approach would be to they do not reflect phylogeny. To use these methods dispense with classification and use the cladogram di- fruitfully, therefore, it would be necessary to follow the rectly to identify the ancestral state for each compo- roundabout way of first making a cladistic analysis and nent. then translating the result into a new classification. One Ridley (1983) proposed a solution for discrete charac- would then make an estimate of the constraining rela- ters. Cladistic methods (parsimony assignments of traits tionships for each level of interest in the cladistic classi- to phylogenies) could be used to count the number of fication: for example, for one family, for each of three times a trait has evolved independently. Felsenstein subfamilies, then for each species in each subfamily. (1985) showed how phylogenies could be used also in Using these average constraints for each level, one comparative studies of quantitative data. The major would then make a prediction of the optimal life history problems with such approaches, of which Grafen's trait as though each of those levels represented a real (1989) "phylogenetic regression" is another example, population of organisms - the average family-level an- are practical. They require that the phylogenies are cestor, the average subfamily-level ancestor and so known. This led Bell (1989) to suggest his comparative forth. Presumably, as more and more precise informa- method, where nested analyses of variance and covari- tion on constraints entered the calculations, the pre- ance are used to partition variance between taxonomic dictions would come closer and closer to the observa- levels, much in the same way as the methods developed tions. This approach to more precise predictions could by Clutton-Brock and Harvey (1977, 1979, 1984) with a be plotted on a graph of predictions vs observations, major difference: for the logical reasons mentioned and the magnitude of changes from family to subfamily above, Bell does not measure correlations between to species would give one a visual impression of the groups but instead within groups. However, his method importance of constraints acting at each level (Fig. 10). still suffers from the problems associated with using There are several problems with this approach, in- non-cladistic classifications or using phylogenies only cluding the assumption that one can actually estimate indirectly as mentioned earlier. the constraint in the putative common ancestor. An- In summary: each method has its own specific draw- other problem is the indirect use of cladograms in this backs - practical or logical. It could be argued, how- and similar methods. Even if cladograms have been ever, that the requirement that the phylogeny should be used to construct the classification, the delimitation of known is not really an argument against a particular families, genera etc. depend on idiosyncrasy. This method. As Felsenstein (1985) remarks: "phylogenies means that one loses much information on relationship are fundamental to comparative biology; there is no and that it becomes difficult to compare relevant clades. doing it without taking them into account".

128 OIKOS 57:1 (1990) Identifyingconvergences Independentderivation of similartraits in differentlin- eages indicateconvergence, one of the strongesttypes of evidence for adaptation. Convergenceis often as- serted without being demonstratedthrough cladistic analysis.Convergence can be demonstratedonly a post- eriori however, (e.g., Coddington1985). After the cla- distic analysishas been performed,it manifestsitself as homoplastictraits that are in conflict with the general cladisticpattern. Purelynumerical techniques could be used, for example, to identifyconvergence in quantita- tive characters.Once convergencehas been identified, one can constructcausal hypotheses by lookingfor simi- Fig. 11. Recent adaptationis "the tip of an iceberg of con- larities in the environment(Telenius et al. 1989). In straint". Stearns' (1983) analysis of life history traits in mam- mals, for example, the similaritybetween beaver and coypuwas striking.These two large, aquaticrodents are Procedure only distantlyrelated cladistically.The similaritiesare thus homoplasies, convergences, which can be ex- Standardphylogenetic checks plained as adaptationsto a shared life style leading to Making certain phylogeneticchecks standardpractice similarselection pressureson life historytraits. would strengthenadaptational analysis. Analysisof coevolution Mitterand Brooks (1983) and Brooks and Mitter(1984) Identifyingcandidates for adaptation suggesteda role for phylogeneticanalysis in studies of In studies focused on one species, cladisticanalysis will supposedlycoevolved and coevolvingspecies. The few identifythose unique traitsthat could be given adapta- studiespublished indicate that historicalconstraints are tional explanationsat this level as autapomorphies.In a widespreadin manygroups but conspicuouslylacking in wider sense, cladisticscan be applied as a tool to refer some. Not enough is yet known to make any strong explanationsto the properphylogenetic level: the level generalizations(see Brooks 1988 for a review). where they appear as apomorphies.Because all traits appearas apomorphiesat some level, a plesiomorphic Cladisticmethods for research trait that is given an historicalexplanation at one level, ecological is of course a candidatefor an adaptationalexplanation Phylogeneticsystematics has developed three sets of at some more general level (where it appears as an techniquesuseful for studies of ecology and evolution: apomorphy). This approach has been underappre- ciated. Its power is neatly exemplified in Wanntorp's discussionof leaf retentionin oaks (1983). Coddington A B C D E A B C D E (1988) discussessuch cladistictests of adaptationalhy- potheses.

Identifyingthe level at whichstatistical independence is attained a In comparativework on two or more species, one AY b shoulddetermine at whatlevel the traitsinvolved can be A B C D E treatedas independentof one another.This point is old (Lack 1968), often repeated (Ridley 1983, 1989, Clut- ton-Brock and Harvey 1984, Felsenstein 1985, Pagel and Harvey 1988), and little heeded. The sum of ances- C tral traits - the "Bauplan"of Gould and Lewontin / d (1979) producingthe "phylogeneticinertia" of Cheve- - Fig. 12. Consensus trees: a and b are two cladograms of the rud et al. (1985) constrainsthe scope of the adaptively same groupof organismsbased on independentdata sets. c is possible at every point in evolution (Brundin 1972). an Adamsconsensus tree, andd is a Nelson, or strictconsensus Some adaptationsthat occurredin the past characterize tree. The Adamstree is completelyresolved, since the resolu- highertaxonomic levels, are integratedinto both geno- tion found in either tree is not contradictedby the (lack of resolutionin the) other. The Nelson tree only acknowledges type and phenotype and function as constraintson the componentCDE, since it is the only part identicalto both lower levels (Fig. 11). trees.

9 OIKOS 57:1 (1990) 129 (1) tree optimization, (2) consensus analysis and (3) associations;those that departfrom the patternshow an parsimony mapping. escape from the historicalconstraints at the point in- dicatedby the incongruence.For a more complete dis- Tree optimization cussion of the technical aspects of mappingmethods, Tree optimizationis used to determinehow manytimes see Brooks (1988), Wiley (1988) and Funk and Brooks and at which points in phylogeny a trait has arisen. (in press). Several methods have been for developed optimizing Conclusions traits on trees, many of which are availableas options on the computerpackages PAUP (Swofford1989) and If ecology and cladistics are to achieve a happy mar- Hennig 86 (Farris1988). They give consistent results, riage, they will have to be able to communicate clearly. differingonly in the way in which they interpretcon- That this might not be straightforward is indicated by vergent and parallel evolution (includingevolutionary the fact that each field is dominatedby differentmetho- reversals).For those interestedin phylogeneticallycon- dological paradigms. If ecology has a central metho- servative traits, this presents no problems. Those in- dology, it is statistics, in particular the analysis of vari- terested in phylogeneticallyplastic traits are often pre- ance and covariance.This predisposesone to think of sented with more than one way to interprettheir data quantitativetraits, normal distributionsand the parti- (Coddington1988). tioning of variance.Cladistics, on the other hand, pre- disposes one to think of qualitative traits, matrices of Consensus trees presence-absencevalues and parsimonioustrees. Thus, Consensus trees provide a summarywhen more than phylogenetic systematics and ecology not only ask qual- one cladogramfor a group is available(e.g., based on itatively different questions - roughly, history and rela- differentdata sets, such as morphologyand behavioural tionship vs process and adaptation - but they also use ecology as in the sticklebackexample above). Consen- qualitatively different methods to get their answers. The sus trees are not valid summmariesof data (Miyamoto initial challenge in developing a methodology that could 1983), but they are excellent for locatingproblem taxa bring the two fields together is, first, to identify ques- and charactersand for highlightingareas of agreement. tions that both methodologies address, and second, to There are two basic types of consensus trees. Adams define clearly how the two methodologies can be cou- consensus trees (Adams 1972) maintainall those por- pled, in all technical detail, to achieve a common an- tions of alternativetrees that do not conflict with each swer to which each has made a significant contribution. other. Nelson consensus trees (Nelson 1979, 1983) Some progress has been made, but much remains to be maintainonly those portionsof alternativetrees that are done. Ecologists who put phylogenetic methods into identical.Fig. 12a,b are alternativecladograms for the their tool-kit will see new problems and turn old ones on same taxa (A-G); Fig. 12c is an Adams consensustree their heads. Systematists that work on organisms im- and Fig. 12d is a Nelson consensus tree (sometimes portant in ecological research will contribute alternative called a strictconsensus tree). explanationsto a sister field and bring rigor to the analysis of adaptation. Parsimony mapping We have stressed the rapprochement of ecology and Species occur in various associations.Geographically- systematics, but that emphasis resulted from the histor- associatedspecies are sympatric.Ecological-associated ical accident that a resurgence of interest in comparative species are synecological,symbiotic or syntopic. Each analysis in ecology coincided with the development of associationis diagnosedby its componentspecies. His- interesting new methods in systematics. In principle, toricaleffects in such associationswill be manifestedin any field of biology with a comparative component patternsof co-variationof the phylogeniesfor the com- stands to gain from introducing the phylogenetic view as ponentgroups. Documenting such co-variation,and de- one of its tools. parturesfrom it, is accomplishedby tree mappingor parsimonymethods (Brooks 1981). In terms of phylo- Acknowledgements- We wish to thank all participantsof the this is "Adaptationand History"workshop at Tovetorpfor a memo- genetic analysis, accomplishedby treating the rableweek in for the frostyspring of 1987. We also wish to thank cladograms the associatedgroups each as a multi- the Nordic Council for Ecology which provided the economic state characterof the association.Each particularasso- means for bringing us all together, and the ethologists of Stock- ciation is treated as a "taxon" (e.g., species A and holm University for generously letting us take over their field species X are sympatricin area III; area III is the taxon, station during that week. and A and X are the characters).The species, plus codes for their phylogeneticrelationships taken from References their cladograms,are used as charactersof the various Adams, E. N. 1972. Consensus techniques and the comparison associations,and a phylogeneticanalysis is performed of taxonomic trees. - Syst. Zool. 21: 390-397. to obtain a for the Bell, G. 1989. A comparative method. - Am. Nat. 133: 553- summarycladogram associations. 571. Those that with to the species co-vary respect summary Berenbaum, M. R. 1983. Coumarins and caterpillars: A case cladogramhave co-varyinghistories with respectto the for coevolution. - Evolution 37: 163-179.

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