Diversity and Evolution of Monocots

Monocots!

Diversity and Evolution We will finish our survey of angiosperms by examining the of Monocots monocots - a lineage of basal angiosperms

Basal angiosperm lineage, but is . . . what, where, when, how . . . appearing to be closer to eudicots than most other basal angiosperms

Monocots! Tremendous economic • Large group: ~ 60,000 species! • Old lineage: ~134 mya importance • Great diversity: habit, habitat, pollination, morphology • Adaptive radiations: (orchids–21,950 spp; grasses–10,035 spp) • Smallest & largest seeds: orchids; Lodoicea maldivica • Largest inflorescences (titan arum, palms, bromeliads) • Smallest fruit, flower & flowering plant (Wolfia)

1 Diversity in ecology Diversity of aquatic habits

emergent • “Trees”, grasses, rosettes, Emergent, floating, or submerged vines, epiphytes… aquatic group of monocots • Carnivores, mycotrophs… These are the first diverging • Habitats: dry, wet, monocots aquatic… • Pollination: water, wind, zoophily submerged

floating

Monocot “trees” Monocot leaves No vascular cambium activity Þ no true secondary growth (wood) • Parallel venation (or Anomalous secondary growth Þ “trees” derived forms) vs. pinnate or reticulate venation as in most dicots • (more on this later)

Dragon tree – a lily relative Woody palm

2 Monocot flower: common theme Diversity in pollination

3-merous Striking modifications & bracts: Tepals are common grasses, pulpits, orchids, spadices & more!

Monocot Origins Monocot Origins

Monocots have usually been Crown group radiation: ~135+ mya [based on DNA evidence] considered as derived out of basal Pollen & leaf: possible early Aptian (Early Cretaceous), 113-125 mya angiosperms - Ranales in the Bessey system or subclass Magnoliidae Oldest unambiguously assigned fossil: Araceae, 110-120 mya with Cronquist

3 2018, Volume 105 • Givnish et al.—Monocot plastid phylogenomics • 9

0.18 PACMAD-BOP Puelioideae Pharoideae Anomochlooideae Monocot Origins Ecdeiocoleaceae Monocot leaf evolution Joinvilleaceae Flagellariaceae Restionaceae s.l. Xyridaceae Poales Eriocaulaceae 0.12 Mayacaceae Cyperaceae Juncaceae Thurniaceae Rapateaceae Typhaceae Bromeliaceae Zingiberaceae • cpDNA genome Costaceae Marantaceae 0.077 Cannaceae Heliconiaceae Zingiberales Strelitziaceae Lowiaceae phylogeny (Givnish et al. Musaceae Pontederiaceae Haemodoraceae Philydraceae Commelinales Commelinaceae Hanguanaceae 2018) 0.029 Arecaceae Arecales Dasypogonaceae Asparagaceae Dasypogonales Amaryllidoideae Allioideae Agapanthoideae Asphodeloideae Hemerocallidoideae Xanthorrhoeoideae Xeronemataceae Iridaceae Doryanthaceae • rapid radiation at base Ixioliriaceae Asparagales Tecophilaeaceae Lanariaceae Hypoxidaceae Asteliaceae Blandfordiaceae Boryaceae Epidendroideae Orchidoideae Cypripedioideae Vanilloideae Apostasioideae Liliaceae Philesiaceae Ripogonaceae • four large burst in species Smilacaceae Classic idea of pre-monocot characteristics – Cronquist’s view: Melanthiaceae Alstroemeriaceae Luzuriagaceae Liliales Colchicaceae Petermanniaceae diversification Campynemataceae Corsiaceae Pandanaceae Cyclanthaceae Tr iuridaceae Pandanales 1. Herbs Stemonaceae Velloziaceae Dioscoreaceae Thismiaceae Taccaceae Dioscoreales Burmanniaceae 2. Aquatic Nartheciaceae Petrosaviaceae Petrosaviales Hydrocharitaceae Nymphaeales Butomaceae Alismataceae Cymodoceaceae Ruppiaceae 3. Perianth not specialized Posidoniaceae Potamogetonaceae Only non-monocot Zosteraceae Maundiaceae Alismatales Juncaginaceae Scheuchzeriaceae 4. Uni-apperturate pollen Aponogetonaceae Tofieldiaceae order with all these other Araceae Lemnoideae Orontoideae Acoraceae Acorales 5. Apocarpy characteristics 140 120 100 80 60 40 20 0 Mya 6. Laminar placentation FIGURE 3. Monocot chronogram/diversigram. Ages of divergence of taxa at the subfamily, family, and ordinal levels of monocots and angiosperm outgroups are shown by branch depth. Signifcant accelerations of diversifcation are identifed by red dots; estimated rates of net species diversifca- tion (sp sp−1 My−1) from BAMM are color- coded as indicated. Area of bubbles is proportional to the number of species in terminal taxa. The Cretaceous- Tertiary boundary is indicated by the dashed line. See Appendix S13 for ages and 95% confdence intervals for all nodes within and among families.

Monocot leaf evolution Monocot leaf evolution

• monocot leaf morphology due to aquatic celery (left) and tomato (right) asterid petioles showing ancestry parallel vascular traces

• monocot leaf is derived from • aquatic è terrestrial è aquatic pathways an expanded bladeless petiole

4 Monocot leaf evolution Monocot leaf evolution Phyllode theory: original monocot lacked a true leaf; only expanded loss of blade petiole variable & expansion expansion of of tissue tissue between between parallel veins parallel veins of petiole in aquatic habitat

Phyllodes: expanded blade-less cross veins & petioles best seen in arid ‘reticulated’ adapted woody legumes such as blades Acacia Acorus sweet flag

Monocot leaf evolution Monocot leaf evolution functional ecological arguments for evolution of broad leaves and fleshy fruits of monocots in shady understory conditions (T. Givnish, 1984, 1999, 2002) loss of blade variable & expansion divergence of tissue of parallel between veins to leaf parallel veins edge of petiole in aquatic habitat

‘parallel-pinnate’ venation of palms and bananas

5 Concerted Concerted convergence convergence

Occurrences of net venation are Occurrences of net venation and overlain on this monocot fleshy fruits are overlain on this phylogeny monocot phylogeny

Both features: • arise multiple times • are correlated with each other • arise in understory clades

Survey of monocots Acorales (*Acoraceae - sweet flag)

4 main groups: • Emergent aquatic plants with ethereal oils and no raphides

• Acorales - sister to all monocots 2 species: • Alismatales Acorus calamus, Old World – inc. Aroids - jack in the pulpit • “Lilioids” (lilies, orchids, yams): A. americanus, New World – non-monophyletic Both species in Wisconsin – petaloid • Commelinids – Arecales – palms – Commelinales – spiderwort – Zingiberales –banana – Poales – pineapple – grasses & sedges Acorus sweet flag

6 *Acoraceae - sweetflag Flat filaments *Acoraceae - sweetflag Flat filaments P 6 A6 G (3) ∞ seeds P 6 A6 G (3) ∞ seeds • Inflorescence with ‘spathe’ and spadix • Inflorescence with ‘spathe’ and spadix • Flowers bisexual • Flowers bisexual

Acorus americanus - sweet flag Acorus americanus - sweet flag

Alismatales Alismatales - aquatics

4 main groups: • Acorales - sister to all monocots Recurring themes: • Alismatales – inc. Aroids - jack in the pulpit Aquatic Þ brackish Þ marine habitats • “Lilioids” (lilies, orchids, yams) – non-monophyletic – petaloid Insect Þ water pollination • Commelinids – Arecales – palms – Commelinales – spiderwort – Zingiberales –banana – Poales – pineapple – grasses & sedges

7 Alismatales - aquatics Alismatales - aquatics

emergent Associated with the aquatic habit is Emergent, floating, or the trend from insect-pollinated, submerged aquatic group showy flowers to water-pollinated, of monocots reduced flowers . . .

and increasing effort to vegetative rather than sexual reproduction submerged

Showy flowers, insect-pollinated

Reduced unisexual flowers, water- floating pollinated

Alismatales - aquatics *Araceae - aroids

72% of Alismatales are unisexual - • Sister family to other Alismatales monoecious or dioecious • Tropical (to temperate)

132 species are hydrophilous (how • epiphytes, herbs, aquatic many origins?) – answer later

Showy flowers, insect-pollinated

Reduced unisexual flowers, water- 104 genera pollinated 2,550 species

8 *Araceae - aroids *Araceae - aroids

• raphides in vacuoles with mucilage Inflorescence a fleshy spadix, surrounded by bract called the • Ca-oxalate (endo-osmosis) spathe CA 0 CO 0 A 6- G (2-3)

Flowers unisexual or perfect Fruits berries clustered on spadix spadix

• defining characteristic is spathe the inflorescence of spathe (cut away) and spadix • spathe (or bract) is common in monocots Symplocarpus foetidus - skunk cabbage Arisaema triphyllum - jack-in-the pulpit

*Araceae - aroids *Araceae - aroids

L:female R:male

Cabbage-like leaves emerge later in the spring Foetid smelling spathe and spadix emerges early in spring or late winter; attracts Symplocarpus foetidus - skunk cabbage carrion flies by heating up Arisaema triphyllum - jack-in-the pulpit [or jill-in-the-pulpit ?] and volatizing off the odor

9 *Araceae - aroids Endogenous heating of skunk cabbage (S. renifolius) spadix

sapromyophily pollination flesh flies – Sarcophagidae

Symplocarpus foetidus - carrion flies – gnats -

skunk cabbage Calliphoridae Mycetophilidae Onda Y. et.al. Plant Physiol. 2008:146:636-645

*Araceae - aroids *Araceae - aroids

Calla palustris - water arum Only emergent aquatic member Monstera - tropical aroid of the family in Great Lakes

10 *Araceae - aroids *Araceae - aroids Zantedeschia other strange aroids: arum lily Amorphophallus - titan arum

Pistia - water lettuce

“Lemnaceae” - duckweeds

funeral plants!

Spathiphyllum

*Araceae (Lemnaceae - duckweeds) *Araceae (Lemnaceae - duckweeds) Floating or submersed aquatic *family* almost cosmopolitan in distribution; Lemna Vegetative reproduction primarily

Now known to be derived from within the Smallest member Araceae of the family and Lemna minor - small duckweed the angiosperms: Wolffia columbiana - Includes the smallest water meal angiosperm, and the smallest flower Spirodela polyrhiza Largest member of the family Inflorescence reduced to 1 great duckweed female and 1-2 male flowers Lemna turionifera - perennial duckweed

11 Tofieldiaceae - asphodels Butomaceae - flowering rush • emergent aquatic family • leaves show no obvious blade and petiole differentiation

• Surprising inclusion! • “Lilioid” flowers (Liliaceae s.l.) • wet loving small herbs Triantha glutinosa

Butomaceae - flowering rush Alismataceae - water plantain • flowers in umbels Aquatic or wetland family, especially in north • unsealed carpels - follicles temperate regions • introduced - invasive Leaves long petioled, often with sagittate- CA 3 CO 3 A 9 G 6 shaped leaves Tubers starchy, often edible

Sagittaria - arrowhead

Butomus umbellatus - flowering rush

12 Alismataceae - water plantain Alismataceae - water plantain

Sagittaria - arrowhead CA 3 CO 3 A 6 - ∞ G 6 - ∞ Sagittaria - arrowhead CA 3 CO 3 A 6 - ∞ G 6 - ∞

Calyx of 3 green sepals, corolla Calyx of 3 green sepals, corolla of 3 white petals of 3 white petals

Apocarpic in a head or ring Apocarpic in a head or ring

Perfect, monoecious, dioecious Achenes (head of achenes here)

Alismataceae - water plantain Potamogetonaceae - pondweed

Aquatic plants with dimorphic leaves, 25 species in Wisconsin difficult to identify, hybridize, and some are troublesome weeds

Similar to Sagittaria, but with carpels in one ring rather than globose head

Alisma plantago-aquatica - water plantain Potomogeton sp. - pondweed

13 Potamogetonaceae - pondweed Potamogetonaceae - pondweed

• perianth of 4 clawed segments if present

• gynoecium typically of 4 free, 1-ovuled carpels

• fruit drupe-like

CA 0,4 CO 0 A 4 G 4 Potomogeton nodosus - pondweed Flowers (top) and fruits (bottom) Potomogeton sp. - pondweed

Hydrocharitaceae - frog bit Hydrocharitaceae - frog bit

• submersed or floating Vallisneria (tapegrasses, eelgrasses) aquatic plants are composed of two species, one New World, one Old World • various forms of water pollination present

Vallisneria americana - tapegrass (with Hydrilla verticillata) Elodea canadensis - waterweed Vallisneria americana - tapegrass

14 Hydrocharitaceae - frog bit Evolution of Sea Grasses

• male flowers in clusters; female flower single Don Les’ story of plants going back to the oceans 450 million years later • pollen water boat floats and attaches to 3 broad stigma of the female flower . . . another story of convergence and • flower retracts and forms fruit under divergence water

Vallisneria spiralis - tapegrass (OW)

Note the floating male flowers and one large female with 3 stigmatic areas on a long peduncle

Vallisneria americana - tapegrass

Evolution of Sea Grasses Evolution of Sea Grasses

Aquatic Þ Salt Tolerant Þ Hydrophily Þ Hydrophily Þ Marine

Aquatic plants found Salt tolerance also Water pollination in most lineages wide-spread restricted Seagrasses found in only one lineage of these aquatic, salt tolerant, and water pollinated lineages (order Alismatales)

Callitriche Ceratophyllum A single origin of seagrasses?

15 Evolution of Sea Grasses Evolution of Sea Grasses

• hydrophily originated 10 • oldest known clonal organism * times in angiosperms * – 200,000 years old ! ** ** • 8 of these times independently ** in Alismatales! **

* * • marine habitat originated 3 * * * * times independently in * * * * Alismatales! * * • marine habitat correlated with hydrophily Posidonia oceanic L.

DNA based tree of Alismatales with water pollination and seagrasses mapped on

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