Zoologica Scripta, Vol. 26, No. 4, pp. 313-322, 1997 Elsevier Science Ltd Pergamon 0 1998 The Norwegian Academy of Science and Letters All rights reserved. Printed in Great Britain PII: S030~3256(98)00008-7 0300-3256/97 $17.00+0.00 Phylogenetic approaches in coevolution and biogeography FREDRIK RONQUIST Accepted 21 January 1998 Ronquist, F. 1998. Phylogenetic approaches in coevolution and biogeography.-Zool. Scr. 26: 313- 322. I review phylogenetic approaches to problems in coevolution and biogeography, illustrating with case studies. In coevolution, genealogical trees are essential in differentiating between ancient and recent associations, in identifying cospeciation events, and in studying host-switching patterns. Cospeciating associations are of particular interest because they allow powerful tests of molecular clocks and accurate comparison of evolutionary rates across groups of organisms. In biogeography, phylogenies can help reconstruct the distribution history of individual groups and identify past geological events that have affected the evolution of entire communities. Parsimony analysis in coevolution and biogeography should be based on identification of different types of events, each of which is associated with a specific cost. Similar event-based methods are applicable to coevol- utionary and biogeographic inference, as well as in the mapping of gene trees onto organism trees. The discussed examples span a variety of organisms and spatiotemporal scales: primate pin worms, HIV, pocket gophers and their lice, aphids and their bacterial symbionts, gall wasps and their host plants, the root of the tree of life, the historical biogeography of the Holarctic, and the geographical origin of our own species. 0 1998 The Norwegian Academy of Science and Letters Fredrik Ronquist, Department of Zoology, Uppsala University, Villavagen 9, SE-752 36 Uppsala, Sweden. Introduction Even if we restrict coevolution to symbioses, in which one organism lives inside or on the surface of another, we The hierarchy of life is the general reference system in are talking about an exceedingly common phenomenon. biology; thus, understanding genealogical relationships is Take, for instance, a normal, healthy, adult human. He fundamental to all biological research. In this paper, I will (or she) carries around about 1.5 kg of microorganisms, in discuss some of the ways in which phylogenetic hypotheses number more than 10 times as many as the cells in the can be used in the study of two, as we shall see, closely body (Grubb 1994). The microorganisms occur on the related biological disciplines: coevolution and biogeo- skin, in the oral cavity, in the outer parts of the urinary graphy. In particular, the basics of parsimony inference in tract, but above all in the intestine. Of bacteria alone there these disciplines will be explained. I will also show how are more than 400 species in the normal gut flora (Grubb coevolutionary methods can be used in the mapping of 1994). We are so intimately adapted to our intestinal flora gene trees onto organism trees. I will argue that parsimony that our well-being is entirely dependent upon it. In methods in coevolutionary and biogeographic inference, addition to the normal flora, humans are associated with like in phylogenetic inference, must be based on the identi- a number of pathogenic viruses, bacteria, and protozoans, fication of different types of events, each of which is as well as parasitic higher animals such as tapeworms, assigned a cost related to the likelihood of that event. roundworms, pin worms, head-lice and itch-mites. We Hence, I will be focusing throughout the paper on event- have no reasons to believe that humans are exceptional; based parsimony methods and neglect many of the other other organisms undoubtedly carry similar communities commonly used methods which cannot, or have not yet, of symbionts and parasites. been described in such terms. With some of our symbionts, we share a long evol- utionary history, dating back long before the time when the human evolutionary lineage separated from that of the chimpanzees. Other organisms have only recently come to Coevolution be associated with humans. How can we separate new- comers from veterans among our associates? Coevolution occurs when two species interact with each To answer this question we need phylogenetic trees. other intimately enough and sufficiently long to affect each Take for instance the pin worm, a common human parasite other’s evolution. Some familiar examples of such co- in temperate areas, particularly among children. Let us evolved species associations include moth larvae and the compare current estimates of relationships among the host plants they feed on, orchids and their pollinators, human pin worm and its closest relatives and our own and termites and their intestinal symbionts that help them genealogical relationships (Fig. 1). If we disregard humans, digest cellulose. all speciations, or branching points, in the pin-worm phy- 313 Zoologica Scripta 26 314 F. Ronquisl pin worms primates - Macaque SIV - Human HIV2 verm. c----- gibbon - Fig. I. Relationships among some primate pin worms and their hosts Human HlVl (6 isol.) (Glen & Brooks 1985; Shoshani et a/. 1996). Dashed lines connect para- sites with their hosts. The parasite phylogeny mirrors the host phylogeny Chimpanzee SIV perfectly, if we assume that the pin worm of humans went extinct and I was replaced by the pin worm of gibbons. Human HlVl (2 isol.) Mandrill SIV logeny correspond to speciations in the primate tree. The only reasonable explanation is that pin worms already plagued the common ancestor of humans and apes, and that they share our evolutionary history. When host popu- lations became isolated and developed into separate spec- ies, the parasites were simultaneously isolated and use phylogenies for one group to elucidate relationships in responded by speciating. Such parasite-host cospeciation the other group. Mitochondria, originally derived from is of particular importance in the study of coevolving free-living bacteria, is a group of symbionts that, in prin- associations. ciple, show strict cospeciation with their host organisms. Humans deviate from the cospeciation pattern (Fig. 1). If this were not so, mitochondria1 genes could not be used We can explain this by assuming that humans originally in the study of relationships among their host organisms. hosted a pin worm that was closely related to the pin worm When the patterns are less clear, quantitative methods of chimpanzees. Later, the pin worm of gibbons colonised are needed to show whether or not there is a nonrandom humans and displaced the original human parasite. Alter- fit between the host and parasite phylogenies. For instance, natively, humans may have escaped pin-worm attack earl- there are many similarities between the phylogenies of ier, before being infected by the gibbon parasite, perhaps pocket gophers, a North American group of ground-dwell- as early as the time when humans and chimpanzees became ing rodents, and their chewing lice (Fig. 3), but there are separately evolving lineages. In either case, phylogenetic also important discrepancies. Can we safely draw the con- trees can help us draw two conclusions. First, pin worms clusion that the lice have cospeciated with their hosts? have been associated with our evolutionary lineage for a A simple type of method we can use in this case is long time, and humans are therefore likely to have ancient parsimony analysis. In its most generalised form, par- defence mechanisms against pin worms. Second, the pin- simony analysis is based on the identification of diffe1ent worm species attacking humans today is a recent colonist types of events, each of which is associated with a cost in evolutionary terms, and we might therefore be less well inversely related to the likelihood of that event. In other equipped to deal with the unique features of this particular words, when we combine events into a solution, rare events species. are costly and likely events cheap. The most parsimonious Take another example, the human immunodeficiency reconstruction is the cheapest combination of events that virus (HIV). It was initially thought that HIV was trans- will solve the problem; if events are assigned costs appro- mitted from monkeys to humans in Africa some decades priately, this is also the most likely explanation of the data. ago, and then rapidly spread over the globe, but recent The simplest type of parsimony analysis of phylogenetic trees of relationships among HIV isolates and related relationships is based on binary characters. There are two viruses give a more complex picture (Fig. 2) (Siddall 1997). different states (0 and 1) and two different types of events There are two, fundamentally different types of HIV. Type (a 0- > 1 change and a 1-> 0 change), each with the same 2 is only found in Africa, whereas type 1 is cosmopolitan. cost. From this, we can calculate the most likely phylo- Phylogenetic analyses show that type 2 is closely related genetic hypothesis, i.e., the tree requiring the smallest num- to viruses occurring in mangobeys. In this case, recent ber of evolutionary changes. transmission to humans appears likely, perhaps through In coevolutionary analysis we need to consider four infected monkeys biting humans (Leigh Brown & Holmes different types of events: duplications, host shifts, sorting 1994). Type 1, however, is closely related to a chimpanzee events, and cospeciations (Fig. 4) (for an overview of isolate, but not to type 2 or other monkey isolates. Thus, coevolutionary methods that are not event-based, see HIV type 1 cannot have evolved from HIV type 2, and it Brooks (1988)). Duplications occur when parasites spe- is quite possible that HIV 1 is a virus that has an ancient ciate independently of their hosts, but remain associated association with humans and only recently became with their ancestral host (Fig. 4A). Host shifts are often strongly virulent (Mindell et 1995). al. considered as being associated with parasite speciation, Parsimony methods one daughter parasite lineage shifting to a new host (Fig.