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Nested in chaos: Insights on the relations of the ‘Nidularioid Complex’ and the evolutionary history of Neoregelia (Bromelioideae-Bromeliaceae)

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Abstract

The ‘Nidularioid Complex’ is a group within the Bromelioideae usually characterized by inflorescences nested within water-impounding foliar rosettes. Currently, it comprises six genera: Canistrum, Canistropsis, Edmundoa, Neoregelia, Nidularium, and Wittrockia. While most of these genera occur in eastern Brazil, the distribution of Neoregelia is disjunct between the Atlantic Rainforest and Amazonia. Previous phylogenetic studies have not addressed the monophyly of and relationships among these genera; therefore, we undertook a phylogenetic study of the Nidularioid Complex with emphasis on the genus Neoregelia and its subgenera. A parsimony-based phylogenetic analysis with 101 morphological characters retrieved the Nidularioid Complex as non-monophyletic. Nidularium and Edmundoa were monophyletic. Neoregelia was recovered as non-monophyletic due to the inclusion within it of the Amazonian subgenus Hylaeaicum. These results highlight the need for revision of the generic classification of Bromelioideae, pending increased sampling of taxa and characters.

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Acknowledgments

This work is part of the MSc. dissertation of AKLV, developed at the Jardim Botânico do Rio de Janeiro. FSS is grateful to CAPES for a doctoral scholarship (Edital MCT/CNPq/MEC/Capes No 52/2010–PROTAX). The authors thank Gustavo Martinelli for providing plant material, Monique F. Neves for assistance in preparing leaf sections, Daniela Zappi for help with content and English writing, and Julián Aguirre-Santoro and an anonymous reviewer for their critics and suggestions that greatly improved the manuscript. RCF is a CNPq research fellow.

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Authors and Affiliations

  1. Jardim Botânico do Rio de Janeiro, Rua Pacheco Leão, 915, Rio de Janeiro, RJ, CEP 22460-030, Brazil

    Fernanda Santos-Silva, Anna Karla L. Venda, André Mantovani & Rafaela Campostrini Forzza

  2. Faculty Centre of Biodiversity, Rennweg 14, 1030, Vienna, Austria

    Heide Marie Hallbritter

  3. Herbarium Bradeanum, P.O Box 15005, CEP20031-970, Rio de Janeiro, RJ, Brazil

    Elton M. C. Leme

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  1. Fernanda Santos-Silva
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  2. Anna Karla L. Venda
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  4. Elton M. C. Leme
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  5. André Mantovani
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Correspondence to Fernanda Santos-Silva or Rafaela Campostrini Forzza.

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Suppl. Material 1

Inflorescence types present in the studied specimens with voucher numbers. A. Neoregelia coimbrae, corymb (RB306979). B. Quesnelia arvensis, spadix (RB338965). C. Canistrum aurantiacum, capitulum (RB330755). D. Aechmea mertensii, spike (RB201814). E. Neoregelia longisepala, closed panicule (corymbform) (RB536616). F. Aechmea echinata, umbel of capitula (RB420012). G. Canistropsis billbergioides, raceme of capitula (RB430452). H. Aechmea caesia, double spike (RB587706). (GIF 255 kb)

High resolution image (TIF 168 mb)

ESM 1

(DOCX 33 kb)

Suppl. Material 3

Accelerated transformation (ACCTRAN) character optimization in one of the most parsimonious trees (MPT 300) of the Nidularioid Complex morphological analysis. Character symbols are shaded as follows: white circles=homoplastic, black circles=non-homoplastic. Numbers above the circles represent character numbers, and those below the circles represent character states. The different subgenera of Neoregelia are coded as follows: black circle=Neoregelia subg. Neoregelia, white square=Neoregelia subg. Longipetalopsis, white triangle=Neoregelia subg. Protoregelia, gray hexagon=Neoregelia subg. Hylaeaicum. (GIF 58 kb)

High resolution image (TIF 30.8 mb)

Appendices

Appendix 1. Specimens used in this study.

Aechmea – A. caesia E. Morren ex Baker: Costa 316 (RB); Martinelli 13365, 10709 (RB); Silva 802 (RB); Wendt 168 (RB). A. capixabae L. B. Sm.: Marquete 3894 (RB); Martinelli 11621, 15640 (RB); Silva 1094 (RB); Vieira 971 (RB). A. echinata (Leme) Leme: Martinelli 15434 (RB). A. mertensii (G. Mey.) Schult. & Schult. f.: Duarte 7033 (RB); Farney 1934 (RB); Forzza 289, 5951 (RB); Pereira 794 (RB); Quinet 1980, 1983 (RB). A. mollis L.B.Sm. Jardim 4840 (RB); A. ramosa Mart. ex Schult. & Schult. f.: Forzza 5251 (RB); Jardim 3157 (RB); Wendt 159 (RB). A. weberi (E. Pereira & Leme) Leme: Martinelli 15419 (RB). Billbergia – B. amoena Lindl.: Almeida 45 (RB), Costa 6 (RB), Forzza 2405 (RB). Bromelia – B. minima Leme & Esteves: Martinelli 16227 (RB); Silva 1253 (RB). B. serra Griseb.: Forzza 2320, 3762, 3765 (RB); Monteiro 232 (RB). Canistropsis – C. billbergioides (Schult. & Schult. f.) Leme: Moreira 223 (RB); C. burchelli (Baker) Leme: Moreira 210 (RB). Canistrum – C. alagoanum Leme & J. A. Siqueira: Martinelli 15337 (RB). C. aurantiacum Morren: Martinelli 15130 (RB). C. guzmanioides Leme: Martinelli 15367 (RB). Edmundoa – E. lindenii (Regel) Leme: Forzza 4465 (RB); E. perplexa (L. B. Sm.) Leme: Martinelli 15939 (RB); Hohenbergia – H. blanchetii E. Morren ex Baker: Silva 61 (RB), Foster 75 (R). Neoregelia subg. Neoregelia – N. carolinae (Beer) L. B. Sm: Martinelli 15508 (RB). N. cathcartii C. F. Reed & Read: Leme 2545 (RBvb live collection JBRJ). N. chlorosticta (Baker) L. B. Sm.: Venda s.n. (RB 506197). N. coimbrae E. Pereira & Leme: H. Lima 6484 (RB). N. concentrica (Vell.) L. B. Sm: Martinelli 1716 (RB). N. crispata Leme: Martinelli 15403 (RB). N. cruenta (R. Graham) L. B. Sm.: Venda s.n. (RB 515588). N. dungsiana E. Pereira: Venda s.n. (RB 515584). N. farinosa (Ule) L. B. Sm.: Faria s.n. (RB 504194). N. johannis (Carrière) L. B. Sm.: Reis 1043 (RB). N. johnsoniae H. Luther: Leme 2568 (RBvb live collection JBRJ). N. kautskyi E. Pereira: Martinelli 15643 (RB). N. laevis (Mez) L. B. Sm.: Martinelli 15859 (RB). N. leprosa L. B. Sm. Martinelli 15709 (RB). N. liliputiana E. Pereira: Amaral s.n. (RBvb 1118). N. lymaniana R. Braga & Sucre: Venda 14 (BHCB, RB). N. macahensis (Ule) L. B. Sm. Martinelli s.n. (RB 508260). N. sarmentosa (Regel) L. B. Sm.: Bocayuva 98 (RB). N. cf. smithii W. Weber: Venda s.n. (RBvb live collection JBRJ). N. spectabilis (T. Moore) L. B. Sm.: Dias-Mello 997 (RB). N. zonata L. B. Sm: Foster 197 (RB). Neoregelia subg. Longipetalopsis Leme–N. bahiana (Ule) L. B. Sm.: Jardim 2553 (RB); Martinelli 2683, 4377, 5527, 11259 (RB). N. diversifolia E. Pereira: Forzza 4981 (RB); Martinelli 15751 (RB). N. ibitipocensis (Leme) Leme: Forzza 3338, 3992 (RB); Martinelli 15317 (RB). N. kerryi Leme: Venda s.n. (RB 515592). N. leucophoea (Baker) L. B. Sm.: Costa 508 (RB); Leme 1107 (HB, RB). N. longipedicellata Leme: Martinelli 16007 (RB). N. mucugensis Leme: Brito 2097 (RB). N. paulistana E. Pereira: Seidel 1078 (RB). N. tenebrosa Leme: Costa s.n. (RB 326175). Neoregelia subg. Protoregelia Leme–N. longisepala E. Pereira & I. A. Penna: Leme 3049 (RB). Neoregelia subg. Hylaeaicum L. B. Sm.–N. eleutheropetala (Ule) L. B. Sm.: Hopkins 1437 (RB); Matteo 109 (RB). N. aff. leviana L. B. Sm.: P. Carauta (RB 186108), Leme 2777 (RBvb 1782, live collection JBRJ) N. margaretae L. B. Sm.: Venda s.n. (E. Leme, private collection, RBvb live collection JBRJ). N. myrmecophila (Ule ex G. Karsten & H. Schenk) L. B. Sm.: Costa 194 (RB). N. tarapotoensis Rauh: Luther s.n. (E. Leme, private collection, RBvb 1780, live collection JBRJ). Nidularium–N. innocentii Leme: Martinelli 15387 (RB). N. itatiaiae L. B. Sm.: Fonseca 3 (RB). N. kautskyanum Leme: Martinelli 15685 (RB). N. meeanum Leme: Moreira 226 (RB). N. utriculosum Ule: Lima 6487 (RB). Portea – P. alatisepala Philcox: Almeida 47 (RB), Kautsky 236 (RB), Martinelli 15414 (RB). Quesnelia–Q. arvensis (Vell) Mez: Forzza 4833 (RB); Martinelli 7789 (RB); Vieira 1202, 1234 (RB). Q. humilis Mez: Ferreira 506 (RB); Leme 3473 (RB); Vieira 950 (RB). Wittrockia–W. cyathiformis (Vell) Leme: Brade 21150 (RB); Heiden 892 (RB); Oliveira 1115 (RB); Sucre 5193 (RB). W. gigantea (Baker) Leme: Forzza 3139, 3600, 4192 (RB); Kolmann 6747, 7585 (RB); Monteiro 29 (RB). W. superba Lindm. Fontoura 161 (RB); Silva 145 (RB).

Appendix 2. Characters and character states used in the cladistic analysis of the Nidularioid Complex.

1. Leaves, phyllotaxy, tank: 0=absent; 1=present. 2. Leaves, phyllotaxy, rosette, general shape (live plants/herbarium specimens): 0=broadly infudibuliform; 1=narrowly infundibuliform 2=tubulose. 3. Leaves, blade, shape: 0=linear; 1=linear-triangular; 2=narrowly oblong; 3=narrowly elliptic; 4=oblanceolate; 5=lanceolate; 6=oblong. 4. Leaves, apex, shape (excluding the projection): 0=attenuate; 1=acute; 2=obtuse; 3=emarginate; 4=rounded. 5. Leaves, apex, projection, shape: 0=absent; 1=apiculate; 2=pungent. 6. Leaves, margin, type: 0=entire; 1=aculeate. 7. Leaves, margin, spines, size: 0=conspicuous; 1=inconspicuous. 8. Leaves, margin, spines, orientation (in the same leaf): 0=antrorse; 1=antrorse and retrorse. 9. Leaves, margin, spines, color: 0=brown; 1=green; 2=red; 3=vinaceous. 10. Leaves, sheath transition to blade: 0=abrupt; 1=tenuous. 11. Leaves, sterile blade, color: 0=green; 1=green with vinaceous or reddish maculae; 2=green with a reddish macula at the apex; 3=completely red. 12. Central leaves, color change during anthesis: 0=absent; 1=present. 13. Leaves, sheath, trichomes: 0=lepidote; 1=pannose. 14. Inflorescence, peduncle, size compared to rosette: 0=included; 1=exceeding the rosette. 15. Inflorescence, peduncle, trichomes: 0=absent; 1=present. 16. Inflorescence, peduncle, trichome, type: 0=velutinous; 1=tomentose; 2=floccose; 3=villous; 4=lepidote; 5=lanuginose. 17. Inflorescence, peduncle, bracts, cover type: 0=completely covered, imbricate; 1=partially covered, lax. 18. Inflorescence, peduncle, color at anthesis: 0=white; 1=red; 2=green; 3=brown. 19. Inflorescence, peduncle, bracts, shape: 0=ovate; 1=oblong; 2=elliptic; 3=lanceolate; 4=linear; 5=widely ovate; 6=narrowly ovate; 7=narrowly elliptic; 8=depressed ovate. 20. Inflorescence, peduncle, bract, apex, shape: 0=attenuate; 1=acuminate; 2=rounded; 3=caudate. 21. Inflorescence, peduncle, bract, apex projection, shape: 0=absent; 1=apiculate; 2=pungent; 3=caudate. 22. Inflorescence, peduncle, bract, trichomes: 0=absent; 1=present. 23. Inflorescence, peduncle, bract, trichome, type: 0=lepidote; 1=tomentose; 2=floccose; 3=villous; 4=lanuginose. 24. Inflorescence, peduncle, bract, margin, type: 0=entire; 1=aculeate. 25. Inflorescence, peduncle, bract, color: 0=stramineous with a red apex; 1=green; 2=vinaceous; 3=white; 4=red; 5=pinkish; 6=brown. 26. Inflorescence, structure: 0=simple; 1=compound. 27. Inflorescence, type: 0=corymb; 1=spadix; 2=capitulum; 3=spike; 4=closed panicule (corymbiform); 5=umbel of capitula; 6=raceme of capitula; 7=double spike. 28. Inflorescence, anthesis, order of flower anthesis: 0=centripetal; 1=unordered; 2=centrifugal. 29. Inflorescence, floral bracts, size: 0=exceeding/equaling the pedicel; 1=exceeding/equaling the ovary; 2=exceeding/equaling the sepal; 3=exceeding/equaling the petal. 30. Inflorescence, floral bracts, color: 0=white; 1=stramineous; 2=red; 3=pinkish; 4=brown; 5=green; 6=yellow. 31. Inflorescence, floral bracts, shape: 0=ovate; 1=oblanceolate; 2=oblong; 3=lanceolate; 4=linear; 5=narrowly elliptic; 6=ovate; 7=narrowly-triangular; 8=elliptic; 9=narrowly-oblong. 32. Inflorescence, floral bracts, margin, type: 0=entire; 1=aculeate. 33. Inflorescence, floral bracts, trichome: 0=absent; 1=present; 34. Inflorescence, floral bracts, trichome, type: 0=lepidote; 1=tomentose; 2=floccose; 3=villous; 4=lanuginose. 35. Inflorescence, floral bracts, trichome, location: 0=apex; 1=whole bract. 36. Inflorescence, floral bracts, keel: 0=absent; 1=present. 37. Inflorescence, floral bracts, apex, shape: 0=acute; 1=attenuate; 2=obtuse; 3=rounded. 38. Inflorescence, floral bracts, apex projection: 0=absent; 1=acuminate; 2=apiculate; 3=pungent. 39. Flower, sepal, symmetry: 0=symmetric; 1=subsymmetric to asymmetric. 40. Flower, sepal, shape: 0=ovate; 1=obovate; 2=lanceolate; 3=linear; 4=oblanceolate. 41. Flower, sepal, color: 0=white; 1=brown; 2=red; 3=green; 4=pinkish; 5=yellow; 6=vinaceous; 7=stramineous. 42. Flower, sepal, trichome: 0=absent; 1=present. 43. Flower, sepal, trichome, type: 0=lepidote; 1=tomentose; 2=floccose; 3=villous; 4=lanuginose. 44. Flower, sepal, trichome, location: 0=apex; 1=whole sepal; 2=base. 45. Flower, sepal, apex, shape: 0=asymmetric; 1=acute; 2=attenuate; 3=rounded; 4=apiculate. 46. Flower, sepal, apex projection, shape: 0=absent; 1=acute; 2=apiculate; 3=caudate; 4=pungent. 47. Flower, sepal, consistency: 0=membranaceous; 1=cartaceous; 2=coriaceous. 48. Flower, sepal, keel: 0=absent; 1=present. 49. Flower, sepal, margin, type: 0=entire; 1=aculeate. 50. Flower, sepal, fusion: 0=free; 1=connate. 51. Flower, sepal, fusion, degree: 0=completely connate; 1=connate only at base. 52. Flower, pedicel: 0=indistinct or absent 1=distinct. 53. Flower, petal, consistency: 0=membranous; 1=cartaceous. 54. Flower, petal, apex blade, color distinction: 0=similar to the blade; 1=distinct to the blade. 55. Flower, petal, blade, color: 0=white; 1=pinkish; 2=purple; 3=green; 4=blue; 5=yellow. 56. Flower, petal, apex, color: 0=lilac; 1=red; 2=purple; 3=pinkish; 4=blue; 5=white; 6=yellow; 7=green; 8=orange. 57. Flower, petal, color, distinction between apex and its margins: 0=margins distinct to the apex; 1=margins equal to the apex. 58. Flower, petal, apex, shape: 0=acute; 1=obtuse; 2=rounded. 59. Flower, petal, position at anthesis: 0=suberect to erect; 1=patent to reflexed; 2=curved inwards. 60. Flower, petal, shape: 0=oblanceolate; 1=oblong; 2=obovate; 3=elliptic; 4=linear; 5=triangular; 6=narrowly obovate; 7=lanceolate; 8=narrowly oblong; 9=narrowly elliptic. 61. Flower, petal, fusion: 0=free; 1=connate. 62. Flower, petal, fusion, degree: 0=connate at base; 1=connate up to 1/3 of the length; 2=connate more than 1/3 of the length. 63. Flower, petal, size: 0=up to 5 cm; 1=upwards from 6 cm. 64. Flower, petal, cucullate apex: 0=absent; 1=present. 65. Flower, petal, petal appendages: 0=absent; 1=present. 66. Flower, petal, appendage, shape: 0=spatulate; 1=fimbriate; 2=cupuliform. 67. Flower, petal, callosity: 0=absent; 1=present. 68. Flower, petal, trichomes: 0=absent; 1=present. 69. Androecium, anther, color at anthesis: 0=white; 1=yellow. 70. Androecium, adnation to petals: 0=adnate; 1=free; 2=three antipetal adnate and three free. 71. Androecium, anther, shape: 0=oblong; 1=sagittate; 2=elliptic; 3=linear; 4=obtuse. 72. Gynoecium, stigma, shape: 0=equally long and wide; 1=longer than wide. 73. Gynoecium, ovary, shape: 0=ovate; 1=elliptic; 2=oblong; 3=obovate; 4=subcylindrical; 5=pyriform. 74. Gynoecium, ovary, furrow: 0=absent; 1=present. 75. Gynoecium, ovary, ovules location along ovary wall without considering type of placentation: 0=at apex; 1=up to half the length; 2=only at half. 76. Anatomy, leaf, adaxial surface, contour 0=smooth to slightly wavy; 1=groovy. 77. Anatomy, leaf, abaxial surface, contour: 0=smooth to slightly wavy; 1=groovy. 78. Anatomy, leaf, epidermis, adaxial surface, shape and thickness of epidermal cells: 0=internal periclinal wall highly thickened, reduced lumen; 1=internal periclinal wall poorly thickened, wide lumen. 79. Anatomy, leaf, epidermis, abaxial surface, shape and thickness of epidermal cells: 0=internal periclinal wall strongly thickened, reduced lumen; 1=internal periclinal wall weakly thickened, wide lumen. 80. Anatomy, leaf, epidermis, scale, pedicle, number of cells: 0=two; 1=more than two. 81. Anatomy, leaf, epidermis, stomata, position compared to remaining epidermal cells: 0=same level; 1=under. 82. Anatomy, leaf, mesophyll, adaxial surface, mechanical hypodermis, thickened cells: 0=absent; 1=with one thickened layer and one or more transition layers; 2=more than one highly thickened layer. 83. Anatomy, leaf, mesophyll, abaxial surface, mechanical hypodermis, thickened cells: 0=absent; 1=with one thickened layer and one or more transition layers; 2=two or more strongly thickened layers. 84. Anatomy, leaf, mesophyll, aquiferous hypodermis, extension: 0=up to the thickness of 1/3 of the leaf blade; 1=more than the thickness of 1/3 of the leaf blade. 85. Anatomy, leaf, mesophyll, aquiferous hypodermis to chlorenchyma, abrupt transition: 0=absent; 1=present. 86. Anatomy, leaf, mesophyll, aquiferous hypodermis, cell shape: 0=rounded; 1=anticlinally elongated. 87. Anatomy, leaf, mesophyll, arm parenchyma, presence: 0=absent; 1=present. 88. Anatomy, leaf, mesophyll, arm parenchyma, arm length: 0=short arms, low lacunosity; 1=long arms, high lacunosity.89. Anatomy, leaf, vascular bundles, fiber cap, presence: 0=absent; 1=present. 90. Anatomy, leaf, mesophyll, parenchyma sheath, radiate disposition, presence: 0=absent; 1=present. 91. Anatomy, leaf, vascular bundle, small bundles, fiber projections: 0=wider than tall; 1=taller than wide. 92. Anatomy, leaf, mesophyll, palisade parenchyma, presence: 0=absent; 1=present. 93. Anatomy, leaf, mesophyll, extravascular fibers, presence: 0=absent; 1=present. 94. Anatomy, leaf, extravascular fibers, position: 0=both faces; 1=only adaxial face; 2=only abaxial face. 95. Anatomy, leaf, adaxial face, mesophyll, number of layers of extravascular fibers: 0=one layer; 1=more than one layer. 96. Anatomy, leaf, abaxial face, mesophyll, number of layers of extravascular fibers: 0=one layer; 1=more than one layer. 97. Androecium, stamen, pollen, pollen aperture type: 0=biporate; 1=sulcate; 2=polyporate; 3=inaperturate. 98. Androecium, stamen, pollen, pollen grain size: 0=40-50 μm; 1=bigger or equal to 60 μm. 99. Androecium, stamen, pollen, exine sculpture: 0=reticulate; 1=foveolate; 2=smooth. 100. Androecium, stamen, pollen, lumen shape of exine sculptures: 0=rounded; 1=polygonal; 2=heterobrocate; 3=perfurate. 101. Androecium, stamen, pollen, exine pores: 0=equal or less than 1/3 of pollen diameter; 1=wider than half of pollen diameter.

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Santos-Silva, F., Venda, A.K.L., Hallbritter, H.M. et al. Nested in chaos: Insights on the relations of the ‘Nidularioid Complex’ and the evolutionary history of Neoregelia (Bromelioideae-Bromeliaceae). Brittonia 69, 133–147 (2017). https://doi.org/10.1007/s12228-017-9460-x

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