Sexual Reproduction in

• Movement onto land is an issue Biology for sexual reproduction in plants - unlike for animals • rely on movement of (1) ,(2) young embryo encased . . . real story of the birds & . . . in a seed (or fruit), or (3) spores and beetles, bugs, butterflies, bats pollination biology seed dispersal

Sexual Reproduction in Plants Coevolution

Pollination and seed/spore dispersal important Coevolution – interactions between two different clades as aspects of biosystematics in plants: selective forces on each other, resulting in adaptations that • Gene flow increase their interdependency • Outcrossing vs. inbreeding • Reproductive isolation Animal-flowering interaction is a classic example of coevolution: • Speciation spore dispersal • Co-speciation (coevolution) pollination biology seed dispersal • Plants evolve elaborate methods to attract animal pollinators • Animals evolve specialized body parts and behaviors that aid plant pollination

1 Coevolution Divergence vs. Convergence • classic example of both divergence and convergence in • insect lineages diversified prior to angiosperms, but co- pollination is the family opted by and responded to by angiosperms • frequent shifts to different “pollination syndromes” from ancestral pollination

V. Grant hummingbird bat

Polemoniaceae aggregata subsp. attenuata tip color = subulata subsp. subulata

Linanthus californicus Ipomopsis arizonica dichotomus Linanthus dianthiflorus

Ipomopsis pumila spiritus

− DNA tree with Linanthus parryae Phlox oklahomensis

Phlox stansburyi Phlox drummondii subsp.Phlox glaberrimadrummondii subsp. interior Phlox maculata subsp. maculata pollinator

Phlox condensata Divergence vs. Convergence Phlox multiflora pollinators Phlox diffusa subsp. formosissima Ipomopsis aggregata subsp. Ipomopsis tenuituba subsp. latiloba Phlox bryoides Ipomopsis aggregata subsp. candida Ipomopsis sancti subsp. multiflora Phlox andicola Ipomopsis aggregata subsp. bridgesii subsp. australis Ipomopsis longiflora subsp. neomexicana Ipomopsis tenuituba Ipomopsis aggregata subsp. aggregata Phlox pilosa subsp. pilosa Phlox roemeriana subsp. spicata Ipomopsis macombii Ipomopsis thurberi mapped onto it Phlox cuspidata Ipomopsis congesta subsp. Phlox pilosa subsp. fulgida Ipomopsis effusa Phlox divaricata Ipomopsis guttata Phlox paniculata • another example is evolution of orchid floral form in Platanthera Microgilia minutiflora Loeseliastrum depressum Phlox stolonifera Langloisia matthewsii Microsteris gracilis Langloisia punctata Phlox dolichantha eremicum subsp. eremicum liniflorus Hummingbird ? Eriastrum wilcoxii of Northern Hemisphere Eriastrum luteum subsp. dasyanthum Eriastrum sapphirinum subsp. sapphirinum Leptosiphon jepsonii subsp. austromontanum ancestral! LeptosiphonLeptosiphon androsaceus bicolor Eriastrum densifolium subsp. sanctorum Eriastrum densifolium Leptosiphon breviculus Loeselia mexicana Loeselia glandulosa subsp. conglomerata latifolia Aliciella hutchinsifolia Gymnosteris parvula pauciflorum Aliciella micromeria Polemonium elegans Polemonium micranthum Aliciella heterostyla Aliciella formosa Polemonium viscosum Aliciella mcvickerae Polemonium molle Aliciella stenothyrsa Polemonium flavum Aliciella pinnatifida Polemonium confertum Aliciella pentstemonoides Polemonium brandegeei Polemoniaceae Polemonium caeruleum Aliciella subnuda Polemonium acutiflorum Aliciella haydenii Polemonium occidentale Acanthogilia gloriosa Polemonium pulcherrimum Fouquieria columnaris Fouquieria splendens Polemonium californicum Fouquieria macdougalii Polemonium delicatum Fouquieria diguetii Polemonium boreale Fouquieria ochoterenae Polemonium vanbruntiae Fouquieria formosa Polemonium reptans Fouquieria fasciculata Cantua pyrifolia Fouquieraceae Allophyllum gilioides Cantua candelilla Allophyllum violaceum Cantua bicolor Allophyllum integrifolium Cantua quercifolia Allophyllum glutinosum Cobaea trianae sister to phlox Allophyllum divaricatum cavanillesii Cobaea penduliflora Collomia biflora Cobaea aschersoniana caruifolia family Collomia macrocalyx Saltugilia splendens subsp. splendens Collomia renacta Saltugilia australis Saltugilia splendens subsp. grantii Collomia mazama capitata subsp. abrotanifolia Collomia rawsoniana Gilia capitata subsp. pedemontana Gilia capitata subsp. mediomontana subsp. achilleifolia autogamy pubescens Gilia nevinii Navarretia fossalis Gilia achilleifolia subsp. multicaulis bat Gilia valdiviensis NavarretiaNavarretia atractyloides hamata subsp. tricolor Gilia laciniata bee NavarretiaNavarretia peninsularis viscidula subsp. leptantha Navarretia leucocephala subsp. minima Navarretia mellita Gilia crassifolia Gilia clokeyi Gilia ophthalmoides Gilia ochroleuca subsp. ochroleuca beetle Navarretia capillaris Gilia ochroleuca subsp. bizonata Gilia mexicana subsp. latiflora Navarretia leptalea subsp. bernardina Gilia jacens Gilia cana Gilia leptantha subsp. purpusii Gilia cana subsp. triceps subsp. tenuiflora Gilia interior Platanthera leucophaea bird Gilia modocensis

Gilia malior

Gilia ochroleuca subsp. exilis Gilia tetrabreccia fly Gilia tweedyi Gilia flavocincta subsp. australis Gilia austrooccidentalis Prairie-fringed orchid moth/hawkmoth

Gilia leptantha subsp. pinetorum

Gilia latiflora subsp. excellens Gilia cana subsp. speciosa butterfly Gilia brecciarum subsp. neglecta long−tounged fly Gilia brecciarum subsp. brecciarum Ph.D. Work by Jeff Rose

2 Divergence vs. Convergence What is Pollination? • DNA relationships indicate remarkable divergent and convergent • Pollination: The transfer of pollen from the male anther to the shifts - 3 separate shifts to nocturnal hawkmoth pollination female , in same plant or between two plants

Platanthera

Evolution of the Evolution of the Flower

Evolution of the flower is linked with evolution of • closed carpel for protection of pollination syndromes and why divergence/convergence is ovules and seeds pervasive in floral features

• bisexual to bring male and female parts closer

• primitive flowers had separate pollen- and carpel-bearing structures such as in Archaefructus (and in all gymnosperms)

Archaefructus Drimys - basal angiosperm

3 Evolution of the Flower Evolution of the Flower

• fusion of carpels into one pistil - • epigyny - protection of • fusion of floral parts - efficient deposition of pollen and ovules from probing animals tubular structures for movement of pollen tubes down restricting nectar access one or few style lobes

Evolution of the Flower Evolution of the Flower

• exotic landing platforms, spurs, nectaries, etc - Placement of both and carpels in the same flower specialization for specific pollinators causes inbreeding - subsequent selection for outcrossing • protogyny or protandry - temporal sequence of anthesis or stigma receptivity 1. female phase 2. male phase

Protogyny in Asimina - pawpaw (Annonaceae)

4 Evolution of the Flower Evolution of the Flower

Placement of both stamens and carpels in the same flower Placement of both stamens and carpels in the same flower causes inbreeding - subsequent selection for outcrossing causes inbreeding - subsequent selection for outcrossing

• self incompatibility - chemical on surface of pollen and • heterostyly - reciprocal stigma/style that prevent pollen tube germination separation of anthers & on the same flower (S allele incompatibility system) stigmas

• unisexuality - reversal back to separate sexes in flowers

Primula - primrose Cucurbita - zucchini

Pollination Syndromes Insect Pollination - Entomophily • morphologically convergent adaptive trends exhibited by Modern insect pollinators the floral features of pollinated plants and, in animal pollination, the mouthpart structure and other flower- • Beetles -- Coleoptera interactive features of the pollinators • Flies -- Diptera

Passive Active • Ants -- Hymenoptera • Butterflies -- 1. Wind - anemophily 3. Animal - zoophily • Moths -- Lepidoptera 2. Water - hydrophily (ornithophily, entomophily) • Bees -- Hymenoptera

Primitive type of insect pollination appears to be beetle or fly pollination

5 ANA Pollination Beetle Pollination

• likely that beetles first visited the female cones of and fed on the pollination droplet exudates

• function of pollination droplet originally for capture of wind-blown pollen — shift as food attractant for beetles as in Welwitschia

Welwitschia

American Journal of Botany January 2009 ANA grade has surprising number of . . . including thermophily (heat to pollination types . . . volatize scents for fly pollination) in Illicium floridanum

Beetle Pollination Beetle Pollination

• beetle flowers usually • beetle flowers are pale or dull in color, but have numerous parts - with strong odor flowers provide stamens, as food for chewing beetles Nuphar - yellow Nuphar - yellow water lily water lily

longitudinal view of beetle flowers illustrating various methods of protecting pistils

6 Beetle Pollination Fly Pollination

• carrion beetle pollination is more advanced - coprophily • carrion/dung flies have special pollination system (sapromyophily) • flowers have spicy, Araceae with no reward - flies attracted to flowers to lay eggs fruity, or rotten smell attracting beetles • flowers brownish/purple, often mottled, with foetid odor

Hydnora africana

Cyclocephala beetles Asarum canadense - wild ginger (Aristolochiaceae)

Fly Pollination Fly Pollination

• two specialist families - Aristolochiaceae (birthwort) and Araceae • two specialist families - Aristolochiaceae (birthwort) and Araceae (arum) (arum)

Aristolochia species

Jack-in-the-pulpit Skunk cabbage Dragon-root

7 Fly Pollination Fly Pollination

• two specialist families - Aristolochiaceae (birthwort) and Araceae • many parasites and saprotrophs utilize carrion flies (arum)

Rafflesia (Rafflesiaceae)

Burmanniaceae

Heliosis (Balanophoraceae) Amorphophallus titanum - titan arum

Fly Pollination Bee & Wasp Pollination

• most important group of flower pollinators • advanced fly pollination can be similar to bee pollination - ecologically similar (“bee flies”) • attracted to flower mainly for food (pollen, nectar, oils, etc.) Syrphid on Anemone Xanthogramma on morning glory

Andrena after pollen Halictid after nectar

Macropis europea on Lysimachia vulgaris • oil is essential for juvenile development

8 Bee & Wasp Pollination Bee & Wasp Pollination

• flowers are white, blue, yellow - generally not red • flowers are white, blue, yellow - generally not red • strong UV light patterns • “nectar guides”

Bee & Wasp Pollination Bee & Wasp Pollination

• flowers are white, blue, yellow - generally not red • flowers are white, blue, yellow - generally not red • strong UV light patterns • strong UV light patterns • “nectar guides” • “nectar guides” • fragrant (perfumes, pheromones) • fragrant (perfumes, pheromones) • poricidal anthers - buzz pollination • poricidal anthers - buzz pollination • zygomorphic often - landing platform Eulaema (euglossine)

Solanum - Solanaceae Perfume industry mint Calceolaria Ophrys

9 Bee & Wasp Pollination Bee & Wasp Pollination

• Some plants take advantage of the sex drive of certain insects Two European bee mimic orchids pollinated by different species of bees

• Mirror or bee mimic orchids - pheromones • Male insect mates with flowers • Orchid pollinated

Ophrys ciliatum - orchid in the Mediterranean pollinated by wasp – Ophrys lutea Ophrys sicula What pollinates this tiger Scolia ciliata Ophrys orchid from Colombia? Mrs. Santa Claus?

Catasetum Pollination Catasetum Pollination

• exotic type of euglossine (Eulaema, Euglossa) bee pollination • male euglossines collect pheromones from flowers • Catasetum orchid flowers unisexual and strongly dimorphic • male Catasetum flowers discharge pollinia (323 cm/sec) • why this strong dimorphism? • euglossine bees learn to avoid male flowers • why do males of different species of Catasetum appear more • female flowers must be different looking to attract the different than do the females? euglossine bees - often upside down requiring new behavior

Male flower Male flower triggered

10 Catasetum Pollination Fig Wasp Pollination • pollination biology drives sexual dimorphism and male-male The pollination biology story of Ficus differentiation and female-female similarity (figs) and their obligate pollinators, the fig wasps, is classic • and explains relative degree of sexual dimorphism within an orchid species • monoecious syconium (Fig. 3) is best studied Catasetum species Male A

Female A similarity in morphology Female B Degree of dimorphism Male B Wt (mg) of pollinia

Fig Wasp Pollination Fig Wasp Pollination • host specificity by female wasps who lay eggs in • DNA cladograms of host (fig) and pollinator (fig wasp) gall forming fig ovaries but pollinate other ovaries show co-speciation or co-evolution

• exceptions occur but generally fit the co- evolution model

• 1 fig wasp species for two closely related fig species geographically separated

• 2 related fig wasp species on one geographically widespread fig species

George Weiblen (University Minnesota)

11 Fig Wasp Pollination

• Multiple inter-continental dispersals of figs and their wasp have started new rounds of co-speciation or co-evolution • Co-evolution of the pantropical figs and their wasp pollinators

Cruad et al. (2012) Co-speciation of figs and fig-wasps. Systematic Biology

Butterfly Pollination Butterfly Pollination Butterflies interact • guided by sight and smell with plants most dramatically in longer- • butterflies can see red and orange lived larval stages flowers • usually shaped as a long tube because of insect’s proboscis – to get nectar • flat - butterflies land

12 Moth Pollination Moth Pollination

• Day-active (diurnal) moths visit flowers similar to that of bees • Night-active (nocturnal) moths visit flowers that are dusk or night blooming, white or pale yellow, fragrant, and with long tubular Hummingbird Clearwing Moths structures for long proboscis • no landing platform - moths hover

Platanthera - prairie fringed orchid

Moth Pollination Bird Pollination - Ornithophily

• Night-active (nocturnal) moths visit flowers that are dusk or night • Birds have a good sense blooming, white or pale yellow, fragrant, and with long tubular of color, they like yellow or structures for long proboscis red flowers… • no landing platform - moths hover • . . . but do not have a good sense of smell, so bird-pollinated flowers usually have little odor Adansonia - Madagascar • Flowers provide fluid nectar in greater quantities than for insects • Hummingbird-pollinated flowers usually have long, tubular corolla • Pollen is large and sticky Brighamia - Hawaii

13 Bird Pollination - Ornithophily Bird Pollination - Ornithophily

• Other birds - Africa, Australia, Hawaii • NOT a one way shift to bird pollination • Convergence is the rule

Collared sunbird

Tawny crowned Van der Niet & Johnson (2012) honeyeater on Yellow plumed Phylogenetic evidence for honeycreepers pollinator driven kangaroo paw honeyeater diversification of angiosperms

Bird Pollination - Ornithophily Bat Pollination - Chiroptirophily

• Read . . . • Night-blooming (nocturnal) • White and aromatic • Robust flowers - bats can cling Musa - banana • Often hanging below crown - access for sonar

Does speciation occur more frequently in hummingbird OR in insect pollinated clades AND how much more (e.g., 2X, 5X, 100X) cactus

baobab

14 Other Mammal Pollination Other Mammal Pollination • Marsupials, mice, primates - rarer • Marsupials, mice, primates - rarer • Humans Ken Wood pollinating Brighamia

Honey possum on Banksia Honey possum on coral gum Neotropical mice

Kinkajou with Ochroma pollen Combretum (Combretaceae)

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