1. + Chapter 20: Coevolution and Mutualism Robert E. Ricklefs The Economy of Nature, Fifth Edition

2. + Introduction The rabbit/myxoma story: rabbits are not native to Australia; a few rabbits were introduced to a ranch in Victoria, Australia, in 1859 within a very few years, hundreds of millions of rabbits ranged throughout the continent, destroying pasturelands and threatening wool production the myxoma virus, introduced in 1950 and spread by mosquitoes, proved to be an effective biological control agent, killing 99.8% of infected rabbits later outbreaks of the virus were less effective - why? 2

3. + Evolution of Resistance in Rabbits Decline in lethality of the myxoma virus in Australia resulted from evolutionary responses in both the rabbit and the virus populations: genetic factors conferring resistance to the disease existed in the rabbit population prior to introduction of the myxoma virus: the myxoma epidemic exerted strong selective pressure for resistance eventually most of the surviving rabbit population consisted of resistant animals 3

4. + Evolution of Hypovirulence in Myxoma Virus Decline in lethality of the myxoma virus in Australia resulted from evolutionary responses in both the rabbit and the virus populations: less virulent strains of virus became more prevalent following initial introduction of the virus to Australia: virus strains that didn’t kill their hosts were more readily dispersed to new hosts (mosquitoes bite only living rabbits) 4

5. + The Rabbit-Myxoma System Today Left alone, the rabbit-myxoma system in Australia would probably evolve to an equilibrial state of benign, endemic disease, as in South America: pest management specialists continue to introduce new, virulent strains to control the rabbit population Contagious diseases spread through the atmosphere or water are less likely to evolve hypovirulence, as they are not dependent on their hosts for dispersal. 5

6. + Coevolution When populations of two or more species interact, each may evolve in response to characteristics of the other that affect its own evolutionary fitness. This process is referred to as coevolution: plants and animals employ structures and behaviors to obtain food and to avoid being eaten or parasitized: much of this diversity is the result of coevolution: natural selection on the means of food procurement and escape 6

7. + Coevolution is mediated by biological agents. The evolutionary effects of biological agents are unlike those of physical factors in two important ways: biological factors stimulate mutual evolutionary responses; adaptations of organisms in response to changes in the physical environment have no effect on that environment biological agents foster diversity of adaptations rather than promoting similarity 7

8. + Convergence In response to biological factors, organisms tend to diversify: organisms specialize, approaching feeding, avoidance of predators and mutually beneficial arrangements in unique ways In contrast, organisms responding to similar physical stresses in the environment tend to evolve similar adaptations: this familiar process is known as convergence 8

9. + Identifying Coevolutionary Responses Coevolution refers strictly to reciprocal evolution between interacting populations: the evolution of strong jaws and associated muscles by hyenas to crack the bones of their prey is not coevolutionary, because the bones of the prey have not evolved to resist being eaten the evolution of the ability of an herbivore to detoxify substances produced by a plant specifically to deter that herbivore is coevolutionary 9

10. + Antagonists evolve in response to each other. Charles Mode coined the term coevolution in a 1958 article in Evolution: Mode’s emphasis was on the development of mathematical models to understand mechanisms for the continual evolution of host and pathogen to evolutionary changes in the other: responses of each organism to the other result in a continual cycling of virulent/avirulent pathogens and susceptible/resistant hosts 10

11. + The Contribution of Ehrlich and Raven In a 1964 article in Evolution, Paul Ehrlich and Peter Raven placed coevolution in a more ecological context: they emphasized empirical patterns, observing that closely related groups of butterflies tend to feed on closely related species of tropical vines, suggestive of a long evolutionary history together: coevolution involved the abilities of butterflies to tolerate the particular chemical defenses of their hosts 11

12. + Coevolution reveals genotype- genotype interactions. Coevolution presupposes that each population contains genetic variation for traits that influence their interaction: studies of coevolution between wheat and wheat pathogens (teliomycetid fungi causing rusts) have revealed genotype-genotype interactions affecting fitnesses of host and pathogen parallel genetic variation in local populations of scale insects and individual ponderosa pine hosts may also represent a genotype-genotype interaction 12

13. + Consumers and resources can achieve an evolutionary equilibrium. A simple model relates the rate of evolution of consumer and resource to the efficiency with which the consumer exploits the resource: the consumer has a decreasing function of evolutionary rate with increasing exploitation: as the prey population is reduced, selective value of further increases in predator efficiency is also reduced the resource has an increasing function of evolutionary rate with increasing exploitation: the selective value of adaptations to avoid predation increase 13

14. + Evolutionary Equilibrium and the Red Queen The simple model of changing rates of evolution of consumer and resource suggests a stable equilibrium at which the rates of evolutionary change of consumer and resource are equal, and the rate of exploitation remains constant: this situation is essentially a stalemate in the evolutionary process, as predicted by the Red Queen hypothesis 14

15. + Competitive ability exhibits genetic variation. Competitive ability should be subject to coevolutionary change: competitive ability cannot be detected by examining traits of individuals, but can be inferred from the outcome of competition experiments conducted by Ayala demonstrate clearly the evolution of competitive ability in populations of fruit flies grown under competitive situations 15

16. + Interspecific competitive ability evolves rapidly at low density. Sparse populations can evolve interspecific competitive ability more rapidly than dense populations. Why? perhaps different and conflicting adaptations determine the outcome of intra- and interspecific competition if so, selection for increased interspecific competitive ability will be stronger in the rarer of two competitors as shown by experiments conducted by Ayala and Pimental, this process can result in a sudden reversal in competitive superiority 16

17. + Traits of competing populations may diverge. If competition is a potent evolutionary force, competitors should have shaped each other’s adaptations: however, observations that related species living together differ in their use of resources is not sufficient evidence for evolution of such differences as the result of competition a way around this objection is to compare species where they live apart (allopatric populations) and together (sympatric populations) 17

18. + Character Displacement If character traits of two closely related species differ more in sympatric regions than in allopatric regions, this pattern may have arisen from strong selective pressure for divergence in sympatry, a process called character displacement: ecologists disagree on the prevalence of character displacement in nature patterns consistent with the operation of character displacement have been observed among Darwin’s finches of the Galápagos Islands 18

19. + Mutualists have complementary functions. Interactions between species that benefit both participants, called mutualisms, can also lead to coevolution: each party is specialized to perform a complementary function for the other a highly coevolved mutualism is seen in lichens, partnerships between algae and fungi: such intimate associations, in which the members form a distinctive entity, are examples of symbioses 19

20. + Trophic Mutualism Trophic mutualisms usually involve partners specialized for obtaining energy and nutrients: typically each partner supplies a limiting nutrient or energy source that the other cannot obtain by itself examples include: Rhizobium and plant roots that form nitrogen-fixing root nodules cellulose-digesting bacteria in the rumens of cows 20

21. + Defensive Mutualism Defensive mutualisms involve species that receive food or shelter from their partners in return for a defensive function: the defensive function may protect one partner against herbivores, predators, or parasites examples include cleaner fish and shrimp in marine ecosystems cleaners remove parasites from other fish and benefit from the food value of the parasites removed 21

22. + Dispersive Mutualism Dispersive mutualisms involve animals that: transport pollen in return for rewards such as nectar: these mutualisms tend to be more restrictive (specialized) as it is in the plant’s interest that pollen be transferred to another plant of the same species transport and disperse seeds in return for the nutritional value of fruits or other structures associated with seeds: these mutualisms tend not to be restrictive, with dispersers usually consuming a variety of fruits and one kind of fruit being eaten by many dispersers 22

23. + Coevolution involves mutual evolutionary responses. Coevolution applies only to reciprocal evolutionary responses between pairs of populations. The term coevolution has sometimes been used broadly to describe the close association of certain species and groups of species in biological communities. Are these examples of coevolution? 23

24. + Are close associations coevolutionary? Do pairs of species undergo reciprocal evolution or do “coevolved” traits arise as responses of populations to selective pressures exerted by a variety of species, followed by ecological sorting? Are species organized into interacting sets based on their adaptations, coevolved or not? 24

25. + Coevolution in ants and aphids? Consider the mutualism (on ironweed plants) in which various species of ants protect aphids and leafhoppers and receive nutritious honeydew in return: smaller ants (Tapinoma) tend to protect aphids and larger ants (Myrmica) tend to protect leafhoppers the two genera of ants rarely co-occur on one plant Is this mutualism coevolved? 25

26. + Coevolution in ants and aphids? The ant-aphid-leafhopper mutualism has all the elements expected of coevolution. Can we be sure the adaptations of the various parties evolved in response to each other? we cannot be sure this is a coevolutionary situation because alternative explanations for the various features of this mutualism exist... 26

27. + Coevolution in ants and aphids? Most insects that suck plant juices produce large quantities of nutritious excreta. Ants are voracious generalists that are likely to attack any insect they encounter. The association of different genera of ants with different honeydew sources may simply reflect different sizes and levels of aggression, evolved in response to unrelated environmental factors. Ants may fail to attack aphids and leafhoppers because ants have evolved to protect other nectar sources, such as flowers and specialized nectaries. 27

28. + The Yucca Moth and the Yucca Yuccas (genus Yucca) and yucca moths (genus Tegeticula) are involved in mutually beneficial and obligatory relationships that have been carefully studied: the approach of phylogenetic reconstruction has been used to address the coevolutionary questions surrounding this mutualism 28

29. + Details of the Yucca/Yucca Moth Mutualism The yucca/yucca moth relationship is obligatory (the moth larvae have no other food source and the yucca plants have no other pollinator): adult female yucca moths carry balls of pollen between yucca flowers by means of specialized mouthparts during pollination, the female moth deposits eggs in the ovary of the yucca flower after the eggs hatch, the developing larvae feed on some of the developing yucca seeds, not exceeding 30% of the seed crop the yucca exerts selective pressure on the moths (through abortion of heavily infested fruits) to limit moth genotypes predisposed to lay large numbers of eggs (cheaters) 29

30. + Is the Yucca/Yucca Moth Mutualism Coevolutionary? Many aspects of the mutualism are present in the phylogenetic lineage of nonmutualistic moths within which Tegeticula evolved: many of of the adaptations (such as host specialization and mating on the host plant) appear to have been present in the moth lineage before the establishment of the mutualism itself, evidence for preadaptation what appear to be coevolved traits may have been preadaptations that were critical to establishment of the mutualism in the first place 30

31. + Summary 1 Interactions among species are major sources of selection and evolutionary response. Coevolution is the interdependent evolution of species that interact ecologically. Evidence of evolutionary changes in consumer-resource systems comes from studies of host-parasitoid interactions. Studies of pathogens of crop plants have revealed the genetic basis for virulence and resistance. 31

32. + Summary 2 Predators and prey can achieve an evolutionary equilibrium. Competition can exert strong selective pressure on competitors. One consequence of such selection may be character displacement. Mutualisms are relationships between species that benefit both. Mutualisms may be trophic, defensive, or dispersive. 32

33. + Summary 3 Phylogenetic analysis allows us to infer the evolutionary history of interspecies interactions A carefully studied case of an obligatory mutualism involves yuccas and their pollinators, yucca moths. Identification of coevolved relationships is difficult, and preadaptations may complicate evolutionary interpretation. 33