Plant-animal interactions Co-evolution? Herbivory Plant defense Pollination Seed dispersal Interactions across the life cycle Conservation: butterflies/host plants Photos: Ricklefs (Economy of Nature), Bradshaw & Schemske, Kalko,

TODAY: Coevolution Definitions and issues – Species Interactions – Evolution by natural selection – Fitness – Coevolution? Pairwise Diffuse Geographic mosaic Examples (a few)

SPECIES INTERACTIONS +/- consumer-resource predator-prey, parasite-host, plant-herbivore - /- competition +/+ mutualism trophic, seed dispersal, pollination, defense

Interacting species may coevolve Biotic selective agents evolve Species act as selective agents on each other’s traits Trait A →A’ Trait X →X’

Biological SELECTIVE Agents 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 physical agents foster convergence

EVOLUTION by natural selection Selection = non random association of FITNESS with traits Response to selection (IF there is a genetic basis to traits) = CHANGE IN GENE FREQUENCY ACROSS GENERATIONS and CHANGE IN TRAIT DISTRIBUTION ACROSS GENERATIONS

FITNESS Representation of your stuff in the future – Send yourself – Send your offspring Survival and reproduction both determine your contribution to genes (and trait distributions) in future population

COEVOLUTION (in the strict sense, Janzen 1980) populations of two or more species interact, traits of each may evolve in response to traits of the other reciprocal selective effects on traits

Coevolution or Association? The term “coevolution” has sometimes been used broadly the close association of certain species and groups of species in biological communities, but…

Pairwise or Diffuse Coevolution? 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?

Classic references Charles Mode (1958) coined the term coevolution – host and pathogen: cycling of virulent/avirulent pathogens and susceptible/resistant hosts Paul Ehrlich and Peter Raven (1964) placed coevolution into an ecological context – closely related groups of butterflies tend to feed on closely related species of plants – specialization is associated with host plant chemistry

Geographic Mosaic Theory (Thompson 2005) Geographic selection mosaics: selection varies among populations because there are geographic differences in how fitness in one species depends upon the distribution of genotypes in another species Coevolutionary hotspots: Interactions are subject to reciprocal selection only within some communities. Broader matrix of coevolutionary coldspots, (where selection is non- reciprocal or where only one of the participants occurs). Trait remixing: The genetic structure of coevolving species changes through new mutations, gene flow across landscapes, random genetic drift, and extinction of local populations (shifting geographic mosaic of coevolution). We study a wide range of interactions from antagonistic to mutualistic. In recent years, we have used interactions as different as those between pollinators and herbaceous plants, mycorrhizal fungi and conifers, and bacteria and bacteriophages to explore how coevolution proceeds in different forms of interaction. All our work is directed toward understanding the links among microevolutionary processes (evolutionary dynamics within local populations), mesoevolutionary processes (geographic mosaics of evolving and coevolving species) and macroevolutionary patterns (the patterns observed among diversifying lineages).

TODAY: Coevolution Definitions and issues – Species Interactions – Evolution by natural selection – Fitness – Coevolution? Pairwise Diffuse Geographic mosaic Examples (a few)

Heliconius butterflies have big eyes The caterpillars feed on Passiflora leaves… HERBIVORY

Passiflora leaf shapes and egg mimics are defensive against a visual herbivore HERBIVORY

Everything is connected: Other vines the rainforest are pollinated by Heliconines! Anguria and Gurania in squash family high canopy vines bright, red tubular flowers with a bright yellow marking the center Heliconius get pollen… using amino acids in egg production Very specialized What about Florida firebush? Photos:

Mimicry complex M. marsaeus M. menophilus M. ludovica Northern Peru throughout South America

Butterflies and host chemistry (Ehrlich and Raven 1964) Papilionidae – Papilio: Rutaceae, Umbelliferae & coumarins Pieridae – Pierinae: Capparidaceae, Cruciferae & mustard oil glucosides Nymphalidae – Danainae: Apocynaceae, Asclepiadaceae & milky juice w/bitter glycosides Libytheidae: Ulmaceae, Rosaceae & ? Lycaenidae: – Lycaenini: diverse families, ant-defended Photos: HERBIVORY

The carrot family includes Queen Anne’s Lace, celery, cilantro, parsley, dill…. Berenbaum found: Evolutionary history of the chemistry : increasing complexity and increasing toxicity and increasingly specialized occurrence ONLY highly specialized insects feed on the most toxic ones These are descended from close relatives that feed on less toxic ones Insect families such as Swallowtail butterflies, that feed on carrot family also feed on distantly related Citrus family… Which also has furanocoumarins! Many plants…subset of these…subset of these Papilio thoas from Peru HERBIVORY

Mutualism (+/+): Interactions between species that benefit both participants Trophic – lichen: partnership between algae and fungi – Rhizobium-plants – Mycorhizzae-plants – wood digesters in rumens…bacteria within ciliates Defensive – ant-plants Dispersive – pollinators-plants – seed dispersers-plants

Trophic Mutualism Trophic mutualisms usually involve partners specialized for obtaining energy and nutrients

Defensive Mutualism Defensive mutualisms involve species that receive food or shelter from their partners in return for a defensive function

Dispersive Mutualism Dispersive mutualisms involve animals that: – transport pollen in return for rewards such as nectar – transport and disperse seeds in return for the nutritional value of fruits or other structures associated with seeds

Mimulus lewisii Bumblebee Mimulus cardinalis Hummingbird Experimental genetics Hybrid genotypes in field assays One gene (YUP) swap = change in pollinator? POLLINATION

Yuccas (Yucca) Yucca moths (Tegeticula) mutually beneficial obligate for both partners phylogenetic analysis moth behaviors selected by plants or pre-adapted? POLLINATION

Moth larvae have no other food source and 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)

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 – host specialization and mating on the host plant – traits 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

phylogenetic analysis

Geographic mosaic: +/+ or +/- ? Greya politella: friend or foe to Lithofragma parviflorum? Photo: data Thompson and Cunningham 2002

Summary…idea of coevolution Interactions among species are major sources of selection Coevolution is the interdependent evolution of species that interact ecologically Consumer-resource systems give abundant examples: host-pathogen, host-parasitoid, plant-herbivore..

Summary: mutualisms Mutualisms are relationships between species that benefit both. Mutualisms may be trophic, defensive, or dispersive. Phylogenetic analysis helps infer the evolutionary history of interspecies interactions Experimental genetics in the field can reveal how plant-animal interactions select for different genes and trait distributions Identification of coevolved relationships is difficult, preadaptations and geographic mosaics may complicate evolutionary interpretation