Chapter 20: Coevolution and Mutualism

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Chapter 20 Coevolution and Mutualism

• Robert E. Ricklefs
• The Economy of Nature, Fifth Edition

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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?

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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

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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 didnt kill their hosts were
  more readily dispersed to new hosts (mosquitoes
  bite only living rabbits)

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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.

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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

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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

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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

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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

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Antagonists evolve in response to each other.

• Charles Mode coined the term coevolution in a
  1958 article in Evolution
• Modes 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

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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

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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

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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

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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

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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

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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

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Traits of competing populations may diverge.

• If competition is a potent evolutionary force,
  competitors should have shaped each others
  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)

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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
  Darwins finches of the Galápagos Islands

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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

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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

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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

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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 plants 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

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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?

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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?

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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?

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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...

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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.

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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

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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)

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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

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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.

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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.

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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.