Lecture 18 - Coevolution and the Red Queen Hypothesis

Coevolution Revisited

  • Coevolution involves reciprocal genetic changes in interacting species due to natural selection pressures each imposes on the other.
  • Interactions can have negative (antagonistic), positive (mutualistic), or neutral (commensal) effects.
  • Commensalism: One species adapts to another without inducing evolutionary change in the latter (e.g., whale barnacles).

Geographic Mosaic Theory of Coevolution (GMTC)

  • GMTC links ecological and evolutionary processes that shape species interactions at a landscape level.
  • It explains limits on coevolutionary processes and variation across landscapes.
  • Three assumptions:
    • Species populations are genetically distinct.
    • Interacting species co-occur in parts of their geographic ranges.
    • Interactions among species differ ecologically across environments (context-dependent).
  • Geographic Selection Mosaic: Interaction outcomes are context dependent (genotype-by-genotype-by-environment interaction).
    • Example: Big blue stem grasses and mycorrhizal fungi; mutualistic when co-evolved locally, antagonistic when mixed from different populations.
  • Coevolutionary Hotspots and Coldspots: Driven by imperfect alignment of species populations.
    • Hotspots: Strong reciprocal coevolution.
    • Coldspots: Interacting species are not present.
    • Example: Garter snakes and toxic newts; toxin expression and snake resistance are higher in coevolutionary hotspots.
  • Non-selective Processes: Trait remixing (genetic drift, mutation, extinction) drives variation among populations.
    • Example: Wild parsnip in New Zealand, introduced without its herbivore enemy; relaxation of certain traits until the herbivore arrives and selection resumes.
  • Interactions are context-dependent, with genotype-by-genotype-by-environment interactions driving variation in coevolution strength across landscapes.

Mutualism

  • Mutualism involves the coevolution of two or more species with reciprocal positive effects on each other.
  • Examples:
    • Insect pollinators and flowering plants
    • Avian pollinators
    • Wasps and figs (symbiotic mutualism)
    • Ants and acacia trees
    • Cleaner wrasse and larger fish
  • Insect Pollinators and Flowering Plants: Darwin's orchid and hawk moth example
    • Exaggerated traits result from reciprocal runaway selection.
    • Constraints exist on trait exaggeration, particularly for pollinators, due to associated costs.
    • Driven by mutualistic interactions where parties maximize fitness benefits, but some conflict exists due to potential for cheating.
  • Plants want reliable pollen dispersal with minimum costs, attracting pollinators using signals.
  • Pollinators want floral rewards (nectar, pollen) quickly and efficiently.
  • Balanced Mutual Exploitation: Each party exploits the other, balanced by mutual benefits.
  • Evolution of traits influences the balance of mutual exploitation.
  • Continuum between:
    • Plant getting pollination without rewards
    • Pollinator taking resources without providing service
  • Examples: Nectar robbing, mimicking orchids, flowers entrapping pollinators.

Bird Pollinators

  • Bird-pollinated plants often have red flowers, signaling to birds sensitive to that spectrum.

Figs and Wasps

  • Tight symbiotic mutualism, with each fig species having specific wasp species.
  • Wasps are sexually dimorphic: Flightless males and winged females.
  • Life cycle:
    • Wasp egg hatches (male or female) inside the fig (synconium).
    • Flightless male fertilizes female within a ghoul, digs a tunnel for her exit.
    • Female, carrying pollen, exits, flies to another receptive fig through a special opening (osteole), lays eggs, and pollinates.

Ants and Acacia Trees

  • Acacia trees in African savannas have thorn-like structures (hollow).
  • Ants live in these structures, protecting the tree from herbivores.
  • Mutual benefit: Habitat for ants, protection for the tree.

Cleaner Wrasse

  • Bluestreak cleaner wrasses form cleaning stations on coral reefs.
  • Larger fish (or turtles, rays) visit to have dead skin and ectoparasites removed.
  • Mutualism: Cleaner wrasse get food, larger fish get parasites removed.

Antagonistic Interactions: Victims and Enemies

  • Predator-prey (lions and buffalo) and host-parasite interactions are antagonistic.
  • Host-parasite: Parasites extract resources without providing benefit to the host.
  • Coevolution of predator and prey:
    • Endless arms race (deer and wolves evolving to be faster).
    • Stable genetic equilibrium (stabilizing influences).
    • Regular fluctuation (punctuated).
    • Extinction of one or both species.

Red Queen Hypothesis

  • Metaphor: "Running to stand still" – constant evolution is needed to maintain relative fitness in a changing environment.
  • Critical for population persistence.
  • Explains the advantage of sexual reproduction at an individual level.
    • Sexual reproduction enables recombination, introducing new genes and responding to changing threats.

Background

  • Coined by Leigh Van Valen to explain extinction rates.
  • Constant extinction rates due to coevolution between competing species leads to continuous creation of new species.
  • Biotic competition, driving coevolutionary arms races, influences extinction and speciation.
  • Later adapted to explain the prevalence of sexual reproduction.

Sexual Reproduction and Parasites

  • Sexual reproduction helps diversify the gene pool, disadvantaging parasites focused on specific genotypes.
  • Recombinations from sexual reproduction eliminate disadvantageous mutations.
  • Sex evolved to combat coevolving enemies (predators, parasites, pathogens).

Three Key Predictions

  1. Sex is most beneficial where there is a high risk of infection.
  2. Pathogens are more likely to attack common phenotypes (especially clonal), while sexual lineages have more diversity.
  3. Individuals in sexually reproducing populations choose mates to maximize offspring diversity.
New Zealand Mud Snail
  • Potamopyrgus antipodarum, a freshwater snail, intermediate host for several parasites.
  • Populations vary in the number of sexual or asexual individuals.
  • Trematode parasite (Microphallus) castrates snails, preventing sexual reproduction.
  • Parasites infect snail after it ingests parasite eggs, which then hatch in the snail's gut, consume parts of the intestine, before moving to the snail's gonads and sterilizing it.
  • Studies show higher frequency of males (sexual reproduction) in shallow lake regions (where ducks and parasites are prevalent) relative to deeper zones (coevolutionary hot spots and cold spots).
Topminnow
  • Poeciliopsis (Polo salad topminnow) from Southwestern US, parasitized by a trematode (Olufeia).
  • Lives in fragmented desert streams, with both asexual and sexual populations.
  • Asexually reproduced fish are clonal, with common phenotypes.
  • Sexually reproducing fish are more diverse, with infrequent phenotypes.
  • During a drought, pools became isolated. In one pool, sexual topminnows went extinct and recolonized slowly, resulting in low genetic diversity and high parasitism levels.
  • Researchers increased genetic diversity and saw a switch in parasite prevalence to the more common clonal phenotype (manipulated genetic diversity because of the sexually reproducing phenotypes added).
  • Benefits of having a sexually reproducing population because it generates that genetic diversity needed to help try and escape or at least protect against the impacts of that pathogen.
Mate Choice
  • Parents maximize offspring fitness with careful mate choice.
  • Even hermaphroditic snails prefer sexual reproduction when possible.
Atlantic Salmon
  • Commercially important species that migrates to the ocean (anadromous).
  • Researchers compared offspring diversity of hatchery salmon (limited mate choice) versus wild salmon (mate choice).
  • Higher parasite prevalence in low-diversity hatchery populations relative to diverse wild populations because they choose who to mate with thus have more diverse diversity in their populations and that conferred a benefit against the enemy.

Stonefly Mimicry: A Recent Example

  • Stonefly (Zelandoperla) is polymorphic; some morphs mimic another species (Austroperla), which produces cyanide and is toxic.
  • Evolutionary hot spots and cold spots drive the evolution of the mimic morph.
  • Forested streams (with insectivorous birds) have a higher prevalence of the mimic.
  • Deforested sites (less predation) have lower levels of the mimic.
  • Predation by birds is a strong evolutionary force for the mimic morph.
  • Plasticine models showed higher attack rates on non-mimic phenotypes in the forested sites.

Conclusion

  • Revisited GMTC.
  • Explored mutualism.
  • Discussed victim-enemy systems and the Red Queen hypothesis.
  • Explained three key tenants supporting the benefits of sexual reproduction against enemies.
  • Presented a practical application of understanding coevolution.