Coevolution of Insects and (Flowering) Plants Charles Darwin called the sudden appearance of flowering plants in the fossil record an “abominable mystery.” Present day ideas about phylogeny are based on comparison of modern forms of flowering plants, fossil evidence and thought. However, the mystery persists because of a dearth of fossil evidence. Molecular genetics is presenting new clues to the evolutionary history of flowering plants Of the some 250,000 species of flowering plants, 70% are insect pollinated. And insects relate to all plants in many other ways (for food, shelter). Insects have obviously played a big role in plant evolution. The rise of the flowering plants has been also tied to climatic change (increases in carbon dioxide from unusually large rock building events), dinosaur browsing and the development of the herbacious habit. Likely all these events played a role. In this presentation we will focus on the characteristics of insects that have helped them relate to plants and specifically look at the way certain types of flowers and certain groups of insects are coevolved. Good resources used in thinking about this presentation and developing it: 1. Coevolution Biol 5401: http://www.d.umn.edu/~tcraig/CoevPollinators.htm 2. The Origins of Insect Pollination & Coevolution of Plants and Insects (by Christine Baillie and Andrea Sullivan): http://aci.mta.ca/Courses/Biology/3451/Christineandrea/Co-evolution.htm http://aci.mta.ca/Courses/Biology/3451/Christineandrea/commonpollinators.htm 3. J. Stein Carter’s, “Coevolution and Pollination” – link next slide: http://biology.clc.uc.edu/courses/bio303/coevolution.htm 4. Thomas Miller’s introductory lecture notes on Insect Physiology gives an interesting overview of insect evolution: http://www.faculty.ucr.edu/~insects/pages/teachingresources/tmlectures/00introduction.html Plus others mentioned in slides Photographs in this presentation © Pearson Education or Fred M. Rhoades unless otherwise listed in notes.

Coevolution Mutual evolutionary influence between two species Insects and flowering plants are coevolved Which group “led” is in contention Generally coevolution is regarded to be a slightly looser relationship among organisms than mutualism. Its the process more than the final product.

Characteristics of Insects Segments fused: Head Compound eyes Mouth parts: sucking, chewing, laping Other paired appendages Thorax 3 pairs of legs Wings: none, 1 or 2 pairs Abdomen “Visera” (reproduction, digestion, etc.) Fig 33.33, part Approximately three quarters of all animals are insects The existing (known) numbers of species in various groups. Insects 751,000 Higher Plants 284,000 Other Animals 281,000 Fungi 69,900 Algae 26,900 Protozoa 30,800 Bacteria 4,800 Viruses 1,000 Most insects have wings. Insects were the first terrestrial animals to fly – flight evolved once in Carboniferous; Pterosaurs learned to fly 70 my later (birds and bats some time after). Flight helps insects to disperse, escape unfavorable environmental changes and predators, and allows insects to find food and new environments. Good insect site, part of “Backyard animals”: http://www.earthfoot.org/backyard/2insect.htm And a nice key to insect orders: http://www.howe.k12.ok.us/~jimaskew/binsect.htm Good source for mouth parts: http://www.ndsu.nodak.edu/entomology/topics/heads.htm [Gary Brewer] some SEMs here: http://ion.eas.asu.edu/index.html Nature of wings used to define insect orders

Characteristics of Insects, cont. Like all arthropods, insects molt Complete metamorphism Larva (feeding) Pupa (metamorph) Adult (reproduction) Incomplete metamorphism Immature look like small adults Gradual increase in size from molt to molt Excellent web site on evolution of insect flight (and other insect facts) at the Hooper Virtual Micropaleontological Museum

Insect diversity Some 30 Orders We will look at the circled ones towards the end. Beetles, flies, bees, butterflies, grasshoppers. Some 30 Orders

Insect evolution Arthropods followed plants onto land Insects evolved on land First insect in Mid Paleozoic (springtail) Insect diversity explosion in Late Paleozoic Plants used for food and shelter Early seed plant pollen a food source? Further coevolution with plants in Mesozoic and Cenozoic Insect evolution is particularly related to plants at the beginning and end. Throughout, insects have filled habitats that were formed by all other organisms. Gillott (1995): Insects began to evolve in the Devonian (Age of Fishes) when land colonization began and continued through the Carboniferous when all existing orders were found in the fossil record except a few.  The few that evolved later are predominantly ectoparasites on mammals and arose with mammals did during the Triassic era.  The only exception is Lepidoptera, one of the most successful insect groups in terms of numbers.  This group is thought to have evolved in close associated with flowering plants during late Mesozoic and Cenozoic.  Types of insect herbivory: foliavores, phloem and xylem sap-suckers, phloem and xylem borers, gall formers, root feeders, pollen feeders, nectar feeders, leaf miners, seed predators, shoot feeders From Resource 4 Jurassic 170 mya (dinosaurs) Triassic 220 mya (ectoparasitic insects on mammals) Permian 250 mya (first flowers, endopterygotes diverge) Carboniferous 310 mya (exopterygote insect orders present) Devonian 370 mya (age of fish, first land Hexapods, Collembola) Cambrian 515 mya (marine arthropods abound)

Plant spores and pollen are wind dispersed Bryophytes Ferns, etc. Pollen: Gymnosperms (conifers, etc.) Exceptions (past and present): A few, unusual mosses – Splachnum Several cycads Several Gnetophyta Most flowering plants (but not all) This slide is just a reminder 70 % of existing flowering plants are insect pollinated

Splachnum moss grows on dung and spores are dispersed by flies. All that is seen here is the end of the sporophytes. This may be a very late adaptation. (or such mosses and insects may have been around in the early Mesozoic on reptile dung?)

Gymnosperms Cycads Gnetophytes Some are pollinated by beetles Some present cycads and gnetophytes are beetle pollinated (most are wind pollinated); It is assumed that the first of these gymnosperms also showed some (beetle) pollination. Background photo of cycad from Univ of Georgia Botany Dept. web site: http://dogwood.botany.uga.edu/greenhouses-cycads.html Inset hypothetical pollination of Dioon (cycad) by beetles. This has been observed but this is a hypothetical longitudinal section of what it would look like http://www.plantapalm.com/vce/biology/pollination.htm Cycads in Univ. of Georgia Botany Dept. Greenhouse Pollination of Dioon (cycad) by beetles

Flower evolution Gymnosperm pollen or ovule predation by beetles Some pollination occurred First flowers Pistils hold ovules Numerous, generalized parts Lots of pollen Later flowers Fusion of parts Tubular Bilateral symmetry More colors

Salmonberry flowers are hummingbird pollinated Benefits to the plants Efficient pollen transfer More outcrossing Salmonberry flowers are hummingbird pollinated

Benefits to the pollinators. 70% of flowers pollinated by insects 30% of flowers pollinated by wind, bats, birds Benefits Pollen rich food source Nectar average ~ 40% sugar No benefit? - Trickery pseudocopulation Charles Darwin. 1862. ON THE VARIOUS CONTRIVANCES BY WHICH BRITISH AND FOREIGN ORCHIDS ARE FERTILISED BY INSECTS [Originally published by] John Murray, Albemarle Street, London: 1862. Fig. VII. OPHRYS APIFERA, OR BEE OPHRYS. a. anther. l l. labellum. A. Side view of flower, with the upper sepal and the two upper petals removed. One pollinium, with its disc still in its pouch, is represented as just falling out of the anther-cell; and the other has fallen almost to its full extent, opposite to the hidden stigmatic surface. B. Pollinium in the position in which it lies embedded. Fraegri and van der Pijl wrote in their classic Principles of Pollination Ecology: "Charles Darwin influenced pollination ecology more deeply than anybody else during the nineteenth century," Bee Ophrys – diagram from Charles Darwin

Important pollinating Insect Orders Coleoptera – Beetles Diptera – Flies Hymenoptera – Bees, Wasps & Ants Lepidoptera – Moths & Butterflies The numbers of species in the largest orders of insects, according to Gillott are: Coleoptera         300,000 Lepidoptera       200,000 Hymenoptera    130,000 Diptera                110,000 Since these numbers add to 740,000, it can be seen that they comprise the bulk of the Class Insecta (with 751,000). 

Coleoptera = “sheath-wings” Beetles (not Beatles) 250,000+ named species Chewing mouthparts Beetle flowers Dull, light color Strong odors: fruity, spicy or fetid Pollen, nectar, other flower parts Phratora beetle head SEM by Alfred Köpf - Sonoma State University Phratora beetle head SEM.jpg - Sonoma State University - Electron micrographs of beetle mouth parts Taken by Alfred Köpf at the Swiss Federal Institute of Technology September 1995 http://www.sonoma.edu/users/r/rank/Bio355/lectures/beetmthpt.html

Magnolia

A basal group Angiosperm – This plant is likely beetle pollinated Amborella, a small shrub with tiny greenish-yellow flowers and red fruit, grows in the wild only on the South Pacific island of New Caledonia. Amborella's primitive features include a lack of vessels for conducting water out of the ground and into its leaves. Current thinking places the base of the angiosperms with plants that have moderate sized flowers with a moderate number of parts. Amborella has now been implicated in most studies as the most primitve living angiosperm! Amborella

Skunk Cabbage, Lysichticum

Blowfly SEMs - “tongue” ↑ Diptera = “two-wings” Flies 85,000+ named species Most attack animals Lapping, sucking or sawing mouthparts Fly flowers (carrion flies) Dull, dark colors Fetid odors (dead meat) Few pollen or nectar rewards Blowfly proboscis & head SEMs - University of Bath http://www.bath.ac.uk/ceos/Insects1.html Blowfly SEMs - “tongue” ↑ ← head

“Carrion Flower” or “Starfish Flower” Stapelia - Carrion Flower/ Starfish Flower – picture found on Georgia Southern University website http://www.bio.gasou.edu/Bio-home/Courses/environmental/leege/BOO/ghseontheweb/pollination/site2.html Stapelia – “Carrion Flower” or “Starfish Flower”

Hymenoptera = “membrane-wings” Bees, Wasps, and Ants 110,000+ named species Chewing & lapping mouthparts Hairy bodies Complex social behavior “Bee” flowers bilaterally symmetrical short fused petal tubes yellows and blues patterns visible in UV nectar guides Honey bee head SEM - University of Bath Good site on bumble bee: http://www.mearns.org.uk/mrssmith/bees/body.htm Honey Bee head SEM - University of Bath http://www.bath.ac.uk/ceos/Insects4.html Bumble bee stealing nectar from a Comfrey flower

Collinsia Collinsia = Blue-eyed Mary Hymenoptera flowers bilaterally symmetrical short tubes yellows and blues; patterns visible in UV nectar guides Collinsia

Viola = Violet Viola

Lepidoptera = “scaly-wings” Moths (nocturnal) & Butterflies (diurnal) 150,000+ named species Sucking mouthparts Butterfly & moth flowers Like bee flowers, but with: Long fused petal tubes Butterfly colors: yellow, red Moth colors: white or pale, fragrant Cabbage Butterfly head SEM - University of Bath http://www.bath.ac.uk/ceos/Insects3.html Butterfly - IUCN - The World Conservation Union UK Committee http://www.iucn-uk.org/default.htm Cabbage Butterfly head SEM - University of Bath

Butterfly on Oregano flowers

Convolvulus “Morning Glory” Moth flowers are dull, light, fragrant, night blooming Convolvulus = Morning Glory; this one a native species on northwest coastal beaches

Odonata Grasshoppers, etc. Not pollinating insects But eat a lot of plant biomass with chewing mouthpart

There are dangers to being a pollinator Crab spider predator - Cryptically colored Remains of a meal at lower right Unsuspecting “bee fly” pollinator gets nabbed for visiting marigold