Pollen morphology of Ephedra (Gnetales) and its evolutionary implications

Abstract

The Ephedra lineage can be traced at least to the Early Cretaceous. Its characteristically polyplicate pollen is well-represented in the fossil record and is frequently used as an indicator of paleoclimate. However, despite previous efforts, knowledge about variation and evolution of ephedroid pollen traits is poor. Here, we document pollen morphology of nearly all extant species of Ephedra, using a combination of scanning electron microscopy (SEM) and light microscopy (LM), and reconstruct ancestral states of key pollen traits. Our results indicate that the ancestral Ephedra pollen type has numerous plicae interspaced by unbranched pseudosulci, while the derived pollen type has branched pseudosulci and (generally) fewer plicae. The derived type is inferred to have evolved independently twice, once along the North American stem branch and once along the Asian stem branch. Pollen of the ancestral type is common in Mesozoic fossil records, especially from the Early Cretaceous, but it is less commonly reported from the Cenozoic. The earliest documentation of the derived pollen type is from the latest Cretaceous, after which it increases strongly in abundance during the Paleogene. The results of the present study have implications for the age of crown group Ephedra as well as for understanding evolution of pollination syndromes in the genus.

Keywords:

• character evolution
• light microscopy
• phylogeny
• polyplicate
• pseudosulci
• scanning electron microscopy
• Welwitschia

Acknowledgements

The authors thank the directors of the herbaria A, ASU, B, BM, BR, CAI, E, F, GB, GH, L, LL, M, MO, MSB, NMC, NY, KAS, PE, RAS, S, TEX, UPS, W and WU for access to plant material, and Wafaa M. Amer (Cairo University), Julien B. Bachelier (State University of New York), Chen Hou and Eva Larsén (Stockholm University) for selecting appropriate specimens, Kjell Jansson (Stockholm University) for laboratory assistance, Reinhard Zetter and Friðgeir Grímsson (University of Vienna) for fruitful discussions and Brian K. Horton (University of Texas at Austin) for sharing fossil material. The authors also wish to thank James A. Doyle and one anonymous reviewer for constructive insights and helpful comments on the paper.

Specimens investigated

Mediterranean species. – Ephedra alata Decne., KH Rechinger 102 (S), AA Anderberg 480 (S), Ibrahim & Mahdi s.n. (S), AbdEaleem s.n. (CAI); E. altissima Desf., A Faure s.n. (S), M Staudinger 6714 (W), H Freitag 35035 (KAS); E. aphylla Forssk., G Samuelsson 2696 (S), F Wettstein 2751 (WU), J Bornmüller 1746 (WU), WM Amer (CAI); E. ciliata Fisch. et C.A.Mey., NT Yakovleva (W), EK Balls 2487 (S), H Handel-Mazetti 973 (WU), JET Aitchison 496537 (GH); E. foeminea Forssk., K Bolinder 542 (S), L Norbäck Ivarsson & O Thureborn s.n. (S), R Pamaninio & R Pichisermolli 139 (L), FS Meyers & JE Dinsmoore 8124 (L), JS Andersen et al. 2098 (S), Bornmüller 1746 (A), O Porch s.n. (WU); E. foliata Boiss et C.A.Mey., B Tiagi s.n. (S), Wendelbo & Assadi 16604 (W), Hedberg & Hedberg 92019A V-60888 (UPS), Thulin & Al-Gifri 9975 (V-096087) 183895 (UPS), PN Parker 3304 (A); E. milleri Freitag et Maier-St., P Hein et al. YP 1110 (B), Miller 7667A (E).

North American species. – Ephedra antisyphilitica Berlandier ex C.A.Mey., HC Hanson 344 (NY), ME Jones 3726 (BR), Hendersoin 62-02a (BR), E Palmer 1292 (GH); E. aspera Engelm., KF Parker 7799 (NY), NH Holmgren 6604 (NY), RD Worthington 13620 (NY), BA Stein 31 (RSA); E. californica S.Watson, FM Reed 5772 (L), C Epling & WM Robinsson s.n. (L), A Carter 3667 (L); E. compacta Rose, DS Corell & IM Johnston 20233 (NY); E. coryi E.L. Reed, SM Ickert-Bond 953 (ASU), DS Corell 32805 (S), DS Corell 32785 (S); E. cutleri Peebles, CT Mason Jr. 2192 (ASU), NH Holmgren 12744 (NY), DE Atha et al. s.n. (NY); E. fasciculata A.Nelson, ME Jones s.n. (RSA), FW Gould 1526 (GH), JH Lehr 2309 (NY), PA Munz 12053 (RSA); E. funerea Coville et C.V.Morton, J Wash & IW Clokey 8224 (NY), LS Rose 67021 (S), CL Hitchcock 12329 (A); E. nevadensis S.Watson, IW Clokey 6509 (S), C Epling & W Robinson (S), P Raven 14251 (WU), LS Rose 58108 (NY), E. pedunculata Engelm. ex S.Watson, Johnston 8847 (TEX, LL), Hendrickson 23183 (TEX, LL), RM Steward 2265 (GH); E. torreyana S.Watson, RW Spellenberg 10204 (NMC), IW Clokey 7816 (NY), E Neese & K Mutz 11414 (NY), Johnston et al. 10578 (F); E. trifurca Torr., RD Worthington 24587 (NY), A Nelson 1619 (NY), MC Johnston et al. 10573 (NY), P Allen (S), CV Hartman 642 (GH); E. viridis Coville, LS Rose 58080 (S), JL Reveal 100 (NY), Neely 4353 (NY), JT Howell 3824 (GH).

South American clade. – Ephedra americana Humb., Bonpl. ex Willd., Gerth s.n. (L), E Günter & O Buchtien (S), RE Fries 1044 (S), M Cardenas 4 (GH); E. boelckei F.A.Roig, Maas et al. 8184 (GB); E. breana Phil., KH Rechinger & W Rechinger 63547 (W), IM Johnston 3613 (GH); E. chilensis C.Presl., C Skottsberg 987 (F), Werdermann 138 (E), Jouffel 2751 (GH); E. frustillata Miers, MP Moreno 236 (NY), JB Hatcher s.n. (NY), LR Parodi 11858 (GH); E. multiflora Phil. ex Stapf, Baines et al. 233 (E), J Chiapella 2344 & E Vitek 09–0359 (W), Johnson 6286 (GH); E. ochreata Miers, A Donat 34 (GB), MP Moreno 433 (NY), RH Fortunato 5413 (NY), W Fischer 15 (GH); E. triandra Tul., J Chiapella 2505 & E Vitek 09–0520 (W), A Cuezzo 1954 (S), K Fiebrig 215 (GH); E. trifurcata Zöllner, O Zöllner 7928 (L); E. tweediana Fisch. et C.A.Mey., R Gallinal 5683 (GH), C Osten 22008 (S), S Venturi 348 (S), JH Hunziker 1648 (S).

Asian clade. – Ephedra distachya L., J Prudhomme 89 (WU), K Bolinder 764 (S), I Rácz et al 35308 (S), Rechinger 53066 (W), Flora Germanica Exsicatae 2325 (GH); E. equisetina Bunge, RC Ching 109 (MO), QR Wu s.n. (MO), KK Andrjoschchenko 4027 (S), E Mokeeva (A); E. gerardiana Wall. ex Florin, P Wendelbo s.n. (WU), Walter Koelz 5310 (S), P Wendelbo s.n. (S), Österreichische Karako Exp. 1039 (W), Stainton, Syes & Williams 813 (E); E. intermedia Schrenk et C.A.Mey., Lindberg 117–1947 (W), W Koeltz 2305e (NY), Y Yang 08070801 (PE), JET Atchison 1122 (GH); E. likiangensis Florin, JF Rock 3694 (NY), G Forrest 5564 (BR); E. lomatolepis Schrenk, II Rusanovick & LA Krai 56 (NY); E. minuta Florin, B Dichore 8457 (MSB), Long et al. 153 (W); E. monosperma J.G.Gmel. ex C.A.Mey., H Freitag 33068 (KAS), Potanin s.n. (BR), CG 81–0152 (BR); E. pachyclada Boiss., KH & F Rechinger 3676 (W), A Danin S-2455 (S), JP Mandaville s.n. (BM); E. regeliana Florin, H Hastman 26 (MSB), GL Webster & E Nasir 5959 (W), GL Webster & E Nasir 5950 (GH); E. sarcocarpa Aitch. et Hemsl., F Rechinger 46054b (W), Ruttner 594 (W), Tsanshakt & Riedel 15977 (W), F Rechinger 46295 (W), Aellen & Estafandri 2786 C-7840 (S); E. saxatilis (Stapf) Royle ex Florin, F Lobblichler 87 (M), CE Parkinson 7077 (S); E. sinica Stapf, E Licent 13523 (S), Y Yang 99531 (PE), W Qingru 9812 (MO); E Licewtak 13523 (A); E. strobilacea Bunge, Supra 3369a (NY), A Michelson 3369b (S), KH Rechinger & F Rechinger 2703 (S), Leonard 5582 (BR); E. transitoria Riedl, V Täckholm et al. 9166 (BR), Doppelbaur 190 (M), Rechinger 8990 (W).

Additional information

Funding

Funding was provided from Stiftelsen Lars Hiertas Minne (to KB) and from the Swedish Research Council VR (to CR).