EEOB 400: Lecture 15 Coevolution Coevolution What is coevolution? Two (or more) species: 1) exert selective pressures on each other, and 2) evolve in response to each other Because each species is evolving in response to the other, one important feature of coevolution is that the selective environment is constantly changing When does coevolution occur? Selective pressure will be strongest when there is a close ecological relationship “Close” ecological relationship = usually specialists rather than generalists Important ecological relationships that give rise to coevolution: 1) predators & prey 2) parasites & hosts 3) mutualists 4) competitors mutualist A competitor A predator + prey parasite + host + + mutualist B - - competitor B Coevolution How do we study coevolution? Like most evolutionary questions, it can be studied at various levels: Adaptations of individuals Interactions between species Broad evolutionary patterns Coadaptation Reciprocal adaptations of two species Could refer to species, adaptations possessed by individuals, genotypes, etc. Lycaenid caterpillars secrete “honeydew” that ants drink Ants defend caterpillars against parasitic wasps Honeydew secretion and defense are coadaptations Does coadaptation demonstrate coevolution? Biologists often have a strict definition of coevolution: evidence of parallel evolution between taxa is required Fig-wasp mutualism Fig trees (Ficus) ~750 tropical species, all of which depend entirely on wasps for pollination Figs are not fruits – they are specialized inflorescences with hundreds of unisexual flowers Fig-wasp mutualism Fig wasps (Agaonidae) Males: suited only for boring holes and mating Females: adaptated for flying, burrowing into figs, and laying eggs in fig oocytes Coadaptations Male Female - Receptive figs produce scents that are specific to a particular pollinator species - Shape of ostiole specific to head shape of particular wasp species (lock-and-key) - Morphology of individual flowers specialized to a particular wasp species Female wasp enters via ostiole and oviposits in female flowers Male flowers Female flowers Flower styles are Pollen different lengths – wasps only oviposit in ones w/ short styles Fig-wasp mutualism Don’t worry… the wasps leave before the fruit is ripe to eat Fig-wasp mutualism Seed dispersal Although pollination is very host-specific, seed dispersal is usually not Over 1200 different vertebrate species are known to eat & disperse fig seeds Accordingly, we would expect fig-disperser coevolution to be much weaker Fig-wasp mutualism A twist to the story…parasitism In addition to pollinating wasps, figs are associated with parasitic wasps Parasitic wasps do not enter the ostiole and do not pollinate the fig’s flowers Instead, they use a long ovipositor to puncture the fig and lay eggs from outside Parasites reduce fitness of figs and pollinator wasps - By ovipositing in flowers that would otherwise produce pollinator wasps - By directly predating pollinator wasps in some species - By ovipositing in flowers that would otherwise produce seed for the fig Fig-wasp mutualism Cophylogeny Congruent phylogenies due to cospeciation – strong evidence for coevolution Cospeciation Host jumping “Missing the boat” Incongruent Congruent Figs Duplication Wasps A statistical method known as phylogenetic reconciliation analysis tests the hypothesis that two phylogenies are more different than expected by chance Fig-wasp mutualism Cospeciation Figs and pollinator wasps show a very high degree of cospeciation Despite pressure from parasitic wasps, fig – pollinator specificity is maintained Indicates a very tight ecological relationship Weiblen & Bush (2002) Mol. Ecol. 11:1573-1578 Fig-wasp mutualism Cospeciation Figs and parasites do not show as strong evidence for cospeciation Host jumping Host duplication “Missing the boat” Weiblen & Bush (2002) Mol. Ecol. 11:1573-1578 Fig-wasp mutualism Figs are coadapted to both pollinators and parasites Figs must balance their own reproductive success against the need to maintain pollinator specificity and reduce impact of parasites Pollinators oviposit from within the fig and into innermost layers of oocytes Some ancestral figs solve this problem by producing flowers with styles of different lengths so at least some will produce seed Parasites oviposit through fig and into outermost layers of oocytes Fig-wasp mutualism Figs are coadapted to both pollinators and parasites Figs must balance their own reproductive success against the need to maintain pollinator specificity and reduce impact of parasites Functional dioecy Some species produce figs with either all long or all short styled flowers A will produce pollen and pollinator eggs, so it is functionally male (= no fig seed) B will produce only seed (and parasite eggs), but to do so it has to smell like A to trick pollinator females into entering This strategy doesn’t eliminate parasitism, but it guarantees that seed will be set Note that mutualism is not all “warm and fuzzy”…mutualists will always try to maximize their benefit (pollination) and minimize their cost (loss of seed production) Plant-insect coevolution Cospeciation in a plant-herbivore system Tetraopes beetles eat milkweed plants in the genus Asclepias cospeciation Plant-insect coevolution Cospeciation in another plant-herbivore system Blepharida beetles eat Bursera plants Becerra (1997) Science Plant Beetle Plant-insect coevolution Cospeciation in another plant-herbivore system Blepharida beetles eat Bursera plants There is a high degree of host-specificity Then why so much host-jumping? Why not cospeciation like in Tetraoptes beetles and milkweed plants? Becerra (1997) Science Plant Beetle Plant-insect coevolution Host specificity is determined by the chemical defenses of the plant Four major chemical classes of plant defenses against herbivory (indicated by colors) These chemical classes do not correspond to plant clades (top) The bottom figure shows beetle phylogeny with branches coded for the chemical type of the host The phylogenies are incongruent because host switching can occur as long as the beetle switches to a new host with chemical defenses to which it is already adapted Becerra (1997) Science Cophylogenies Congruent phylogenies can arise for more than one reason Today we are discussing congruence as a result of cospeciation But recall that congruence is also predicted by vicariance biogeography A B C D E Congruent Incongruent Congruent Plant-pollinator coevolution Flower and fly or moth pollinators Many flies and moths have outlandish proboscises to extract nectar from similarly outlandish flowers Darwin received a specimen of the orchid Angraecum sesquipedale and predicted from it that there must exist a pollinator with a proboscis measuring 10-12” This prediction was not confirmed until 1903 with Xanthopan morgani moth Plant-pollinator coevolution Host specificity drives coevolution A flower “wants” its pollen spread to other flowers of the same species A coevolutionary escalation Extravagant traits can coevolve in response Flower evolves Fly responds Plant-pollinator coevolution Mutualisms can be exploited Mutualisms can be exploited by “cheaters” that collect benefits but avoid costs, as in the case of the deceptive orchid Disa nivea D. nivea mimics a nectar-producing flower to fool the fly Prosoeca ganglbaueri Figs 2-4 = flower species that produces nectar Figs 5-6 = mimic orchid that “cheats” Anderson et al. (2005) Am. J. Botany 92: 1342 Ant mutualisms Ants and insects that produce “honeydew” Ants participate in dozens of mutualisms and show coadaptations for each Ants tending a lycaenid caterpillar Ant drinking honeydew from an aphid Many different insects provide ants with “honeydew” – source of nutrition for the ants that has no other function for the insect – specifically coevolved for ants In return, ants defend insects from parasites and predators Ant mutualisms Ants and acacia trees Pseudomyrmex ants protect acacia trees from herbivores – in return, the acacia feeds the ant with nectar and protein rich Beltian bodies, and provides a place for the ants to live in the acacia’s modified thorns Ant mutualisms Ant-fungus mutualism Attine ants (~210 species) have cultivated fungal gardens for over 50 million years Benefits to the ant: Fungi produce nutritional “gongylidia” that are harvested by ants to feed their larvae Fungi can digest cellulose, ants can not Atta cephalotes collecting leaf cuttings for their fungal garden Benefits to the fungi: Ants remove plants and other fungi that compete for nutrients and provision fungi with leaves Ants cultivate actinomycete bacteria that produce antiboiotics against Escovopsis fungi, which would otherwise parasitize the mutualist fungi Ant with pockets of bacteria Captive colony of Atta mexicana tending to a fungal garden Ant mutualisms Ant-fungus mutualism To simplify the system in a diagram: Mutualism Ant Mutualism or commensalism + + - + + Bacterium (actinomycete) Cultivar (gardened fungus) Antibiotics kill parasite Parasite kills cultivar Parasite (Escovopsis fungi) A four-way symbiosis – but do these species coevolve? Ant mutualisms Coevolution – Patterns of parallel evolution between ants and fungal cultivars …and between these two groups and Escovopsis parasites !! Currie et al. (2003) Science 299: 386-388 Host-parasite coevolution Coevolution – Thus far we have seen examples from mutualism interactions Pocket gophers (Geomyidae) are are parasitized by lice (Mallophaga) Clear pattern of cospeciation – this example also shows how rates of evolution can be compared (b) to provide further evidence for coevolution (letters in b = branches in a) Coevolutionary arms races “Arms race” Coevolving species have to constantly “improve” to meet each new adaptation with a “better” adaptation of their own Escalation Coadaptations become increasingly powerful, yet species are not any better adapted because the selective landscape is constantly changing This may sound familiar: it is Van Valen’s Red Queen Hypothesis: - running as fast as possible just to stay in the same place An inherent feature of coevolution We often think of “arms races” as occurring between predators and prey, or between parasites and hosts – this makes intuitive sense But it is not really that different in mutualists – each mutualist will be best adapted when it receives the maximum benefit while paying the minimal cost Coevolutionary arms races An arms race in a predator-prey interaction Taricha granulosa newts have powerful tetrodotoxins (TTX) that are secreted as protection from predators Thamnophis sirtalis garter snakes are the only major predator of this newt – they have evolved resistance to TTX Escalation Toxins produced by newts are hundreds of times more powerful that necessary to kill any other predator (including humans), but snakes are resistant Can we find evidence for coevolution? Brodie et al. (2002) Evolution 56:2067-2082 Coevolutionary arms races Snake populations vary in resistance to newt toxins Snake populations outside of newt’s range have low resistance Brodie et al. (2002) Evolution 56:2067-2082 A geographic mosaic with two coevolutionary “hotspots” Coevolutionary arms races An arms race in a predator-prey interaction The extremely high toxicity of Taricha granulosa, which is hundreds of times more toxic than necessary for most predators, is a result of an escalating arms race with one species, Thamnophis sirtalis Snake resistance is predicted by newt toxicity, as expected if these species are coevolving Brodie et al. (2002) Evolution 56:2067-2082 Evidence for coevolution Local coadaptation Snakes and newts are locally coadapted: - snakes have not evolved resistance in populations outside of the newt’s range - populations with high newt toxicity have high snake resistance Snails and their castrating trematode parasites In three separate studies, parasites were better able to infect snails from their own population than hosts from other populations – parasites are locally coadapted Curt Lively’s research: http://www.indiana.edu/~curtweb/Research/local_adaptation.html Inferring an arms race from fossils Shells of fossil gastropods Difficult to infer coadaptation from fossils because we can’t observe interactions But we can use characteristics that reflect predator-prey interactions When a shell is repaired following a failed predation attempt, it leaves a clear pattern evident in fossils Gastropods “cement” themselves to the substrate as an adaptation against predators Gastropods with thickened or narrowed apertures are better able to survive predation events The incidence of shell repair increases through time, suggesting predation is becoming more intense The incidence of mobile gastropods that lack a means of attachment decreases over time The incidence of thickened or narrowed apertures increases over time Fossils and the Red Queen Probability of extinction The fossil record also supports another important theoretical point: Probability of extinction is constant through the course of evolution Why is this important? It shows that evolution is not progressive – taxa that have been around longer have not become “better adapted” and thus better able to avoid extinction Supports the Red Queen model and implicates coevolution as a major force: Organisms have to keep running (evolving) just to stay in place (avoid extinction) Coevolution and radiation Biologist JBS Haldane was once asked by theologians: “What could one conclude about the Creator from a study of His creation?” Haldane’s reply: “An inordinate fondness for beetles" Coevolution and radiation Why are beetles so speciose? Over half of all beetles are phytophagous (feed on plants), and a large number of these herbivorous beetles feed on angiosperms (flowering plants) Farrell (1998) hypothesized that specialization on different angiosperm species led to the radiation of beetle species The increase in herbivorous beetle genera correlates with the exponential increase of angiosperms beginning in the Cretaceous Radiation of angiosperms Farrell (1998) Science 281: 555-559 Coevolution and radiation Why are beetles so speciose? Phytophagous beetles are a monophyletic group, but specialized feeding on angiosperms has evolved multiple times within phytophagous beetles (A) Curculionoidea (B) Chrysomeloidea Beetles feed on: Cycads Conifers Angiosperms (dicots) Angiosperms (monocots) Many more beetle genera occur in clades that feed on angiosperms Farrell (1998) Science 281: 555-559 Coevolution and radiation Why are beetles so speciose? Specialization on angiosperms leads to rapid beetle speciation via coevolution Evolutionary changes in plant host lead to incredible beetle radiations It is important to note that this same pattern is observed in five different clades, indicating that the change in host type is driving this pattern Radiation of angiosperms Farrell (1998) Science 281: 555-559 Coevolution Why is coevolution important? We can simplify ecology as consisting of 2 types of interactions 1) Abiotic – interactions with temperature, light, nutrients, humidity, etc. 2) Biotic – interactions with other organisms Coevolution occurs only as a direct result of biotic interactions A simple question about the importance of coevolution: If change in the physical environment ceased, would evolution come to a stop?