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Phylogenetic Analyses of Cretaceous Fossils Related to Chloranthaceae and their Evolutionary Implications

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Abstract

Chloranthaceae were one of the first common lines during the early radiation of angiosperms, possibly reflecting adaptation to more open habitats. Phylogenetic analyses clarify the position of Cretaceous mesofossils in molecular trees of Recent taxa. Plants that produced Asteropollis pollen, with tepals adnate to a single carpel, are nested in crown group Chloranthaceae with Hedyosmum; Canrightiopsis, with three stamens and no perianth, is sister to Sarcandra and Chloranthus; and Canrightia is a stem relative that illustrates a still bisexual stage in floral reduction. Plants that produced Pennipollis pollen are related to Chloranthaceae and/or Ceratophyllum rather than monocots. Appomattoxia, which produced Tucanopollis pollen, has equivocal affinities, but Pseudoasterophyllites, with similar pollen and stems with reduced leaves, may be a link between Chloranthaceae and Ceratophyllum. These results imply that flowers became unisexual before losing the perianth, while bisexual flowers in Canrightiopsis, Sarcandra, and Chloranthus are secondarily derived from unisexual flowers.

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Acknowledgements

We thank Alejandra Gandolfo and Elizabeth Hermsen for inviting us to present a talk at the International Palaeontology Congress in Mendoza, Argentina (2014), on which this paper is based; Cuong Nguyen for hosting JAD at Cuc Phuong National Park; Paulo Schwirkowski for providing a photograph of Hedyosmum brasiliense; and two anonymous reviewers for useful comments on the manuscript.

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  1. Department of Evolution and Ecology, University of California, Davis, CA, 95616, USA

    James A. Doyle

  2. Department of Systematic and Evolutionary Botany, University of Zurich, 8008, Zurich, Switzerland

    Peter K. Endress

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Correspondence to James A. Doyle.

Appendix: Phylogenetic analysis of Canrightiopsis

Appendix: Phylogenetic analysis of Canrightiopsis

The data set used to evaluate the position of Canrightiopsis is that of Kvaček et al. (2016), including all potential fossil relatives of Chloranthaceae (except Chloranthistemon) treated in this paper (Table 1). Sources of data on other living and fossil taxa and the rationale for character definitions and scoring of difficult cases are discussed in Doyle and Endress (2000, 2010, 2014), Doyle et al. (2008), Endress and Doyle (2009), and Kvaček et al. (2016). In the following character list we have noted changes made between Doyle and Endress (2014) and Kvaček et al. (2016) that are most likely to affect inferred relationships of Chloranthaceae and potential relatives. We score Canrightiopsis as a consensus of the three species C. intermedia, C. crassitesta, and C. dinisii of Friis et al. (2015), whose preserved features do not differ in any of the characters in our data set; the differences among them are largely quantitative. These species are represented by isolated fruits with stamen scars (but no stamens), enclosed seeds, and adhering pollen.

Table 1 Data matrix used for analysis of the positions of Canrightiopsis and other fossil taxa
Full size table

Characters

Character states scored for Canrightia are indicated in bold font. Uncertain scorings (e.g., 0/1) are shown by putting both states in bold font. When no state is in bold font, the character is scored as unknown (including inapplicable).

1–41 Vegetative characters: unknown; see Kvaček et al. (2016).

42 Inflorescence (0) solitary flower (or occasionally with 1–2 lateral flowers), (1) botryoid, panicle, or thyrsoid (monotelic), (2) raceme, spike, or thyrse (polytelic).

43 Inflorescence partial units (0) single flowers, (1) cymes.

44 Inflorescence (or partial inflorescence) (0) not modified, (1) modified into globular head.

45 Pedicel (0) present in some or all flowers, (1) absent or highly reduced (flower sessile or subsessile).

46 Floral subtending bracts (0) present, (1) present in female, absent in male flowers, (2) absent in all flowers.

47 Sex of flowers (0) bisexual, (1) unisexual. Although Kvaček and Friis (2010) assumed that Zlatkocarpus had unisexual flowers, and we scored it accordingly in Doyle and Endress (2014), Friis et al. (2015) scored Zlatkocarpus as unknown. However, we assume that if Zlatkocarpus was bisexual there would be visible remnants or scars of stamens below or on the fruits, as there are in Canrightia, Canrightiopsis, Sarcandra, and Chloranthus.

48. Inflorescences of unisexual flowers (0) both sexes with more than one flower, (1) male with more than one flower, female with one flower (uniflorous, solitary). Bisexual taxa scored as unknown.

49 Floral base (0) no hypanthium, superior ovary, (1) hypanthium, superior, (2) inferior ovary. See Kvaček et al. (2016) for rescoring of Sarcandra and Chloranthus as inferior. Friis et al. (2015) used a character that distinguished partly epigynous from epigynous, but this is not likely to be informative for placement of Canrightiopsis among Chloranthaceae and related fossils, since only Hedyosmum and the Asteropollis plant are fully epigynous.

50 Floral receptacle (female portion) (0) short, (1) elongate.

51 Pits in receptacle bearing individual carpels (0) absent, (1) present.

52 Cortical vascular system (0) absent or supplying perianth only, (1) supplying androecium, (2) supplying androecium plus gynoecium.

53 Floral apex (0) used up after production of carpels, (1) protruding in mature flower. Not applicable in taxa with one carpel.

54 Perianth (0) present, (1) absent.

55–61 Perianth organization, features of perianth parts: inapplicable; see Kvaček et al. (2016).

62 Calyptra derived from the last one or two bracteate organs below the flower (0) absent, (1) present.

63 Stamen number (0) more than one, (1) one.

64 Androecium phyllotaxis (0) spiral, (1) whorled. Because of the uneven, one-sided position of the three stamens, we consider characters 64 and 65 inapplicable in Canrightiopsis.

65 Androecium merism (0) trimerous, (1) dimerous, (2) polymerous.

66 Stamen whorls (series when phyllotaxis is spiral; includes inner staminodes) (0) one, (1) two, (2) more than two. See Kvaček et al. (2016) for rescoring of Ascarina as unknown for characters 66 and 67.

67 Stamen positions (0) single, (1) double (at least in outer whorl). Inapplicable with one whorl of stamens.

68 Stamen fusion (0) free, (1) connate.

69 Inner staminodes (0) absent, (1) present. Inapplicable with one whorl of stamens; see Kvaček et al. (2016) for rescoring of Canrightia as unknown.

70–81 Stamen morphology, pollen development: unknown; see Kvaček et al. (2016).

82 Pollen unit (0) monads, (1) tetrads.

83 Pollen size (average) (0) large (> 50 μm), (1) medium (20–50 μm), (2) small (< 20 μm).

84 Pollen shape (0) boat-shaped, (1) globose, (2) triangular, angulaperturate.

85 Aperture type (0) single (presumably polar, including monosulcate and monoporate) or disulcate (one furrow at each pole), (1) inaperturate, (2) sulculate, (3) (syn)tricolpate with colpi arranged according to Garside’s law (with or without alternating colpi), (4) tricolpate.

86 Single aperture shape (0) elongate, (1) round.

87 Single aperture branching (0) unbranched, (1) with several branches.

88 Infratectum (0) granular (including “atectate”), (1) intermediate, (2) columellar; ordered.

89 Tectum (0) continuous or microperforate, (1) perforate (foveolate) to semitectate (e.g., reticulate), (2) reduced (not distinguishable from underlying granules).

90 Grading of reticulum (0) uniform, (1) finer at ends of sulcus (liliaceous), (2) finer at poles (rouseoid). Applicable only in taxa with state 1 in character 89.

91 Striate muri (0) absent, (1) present.

92 Supratectal spinules (smaller than the width of tectal muri in perforate and semitectate taxa; includes rounded as well as pointed elements) (0) absent, (1) present.

93 Prominent spines (larger than spinules, easily visible with light microscopy) (0) absent, (1) present.

94 Aperture membrane (0) smooth, (1) sculptured.

95 Extra-apertural nexine (0) foot layer, not consistently foliated, distinctly staining endexine absent or only discontinous traces, (1) foot layer and distinctly staining, continous endexine, or endexine only, (2) all or in part foliated, not distinctly staining.

96 Nexine thickness (0) absent or discontinuous traces, (1) thin but continuous, (2) thick (1/3 or more of total exine); ordered.

97 Carpel number (0) one, (1) two–five in one whorl or series (when spiral), (2) more than five in one whorl or series, (3) more than one whorl or series.

98 Carpel form (0) ascidiate up to stigma, (1) intermediate (both plicate and ascidiate zones below the stigma) with ovule(s) in the ascidiate zone, (2) completely plicate, or intermediate with some or all ovule(s) in the plicate zone. Because developmental or anatomical evidence is often needed to distinguish these states, we have scored this character as unknown in fossils, except when they have a clear ventral slit.

99 Postgenital sealing of carpel (0) none, (1) partial, (2) complete.

100 Secretion in area of carpel sealing (0) present, (1) absent.

101 Pollen tube transmitting tissue (0) not prominently differentiated, (1) one cell layer prominently differentiated, (2) more than one cell layer prominently differentiated.

102 Style (0) absent (stigma sessile or capitate), (1) present (elongated, distinctly constricted apical portion of carpel).

103 Stigma (0) extended (half or more of style-stigma zone), (1) restricted (above slit or around its upper part). In contrast to many fossils, the stigmatic zone in Canrightiopsis is distinct and similar to that in Sarcandra and Chloranthus.

104 Multicellular stigmatic protuberances or undulations (0) absent, (1) present. Characters 104 and 105 are not visible from the surface because of the abundant stigmatic secretion.

105 Stigmatic papillae (most elaborate type) (0) absent, (1) unicellular or with single emergent cell and one or more small basal cells, (2) uniseriate pluricellular with emergent portion consisting of two or more cells.

106 Extragynoecial compitum (0) absent, (1) present. Characters 106 and 107 are not applicable in unicarpellate taxa.

107 Carpel fusion (0) apocarpous, (1) parasyncarpous, (2) eusyncarpous (at least basally).

108 Oil cells in carpels (0) absent or internal, (1) intrusive. Inapplicable in taxa with no oil cells anywhere in the plant. Compared by Friis et al. (2015) with the intrusive oil cells of Chloranthus spicatus.

109 Long unicellular hairs on and/or between carpels (0) absent, (1) present. Characters 109–112 are usually not scored in fossils.

110 Short curved appressed unlignified hairs with up to two short basal cells and one long apical cell on carpels (0) absent, (1) present.

111 Nectary on dorsal or lateral sides of carpel or pistillode (0) absent, (1) present.

112 Septal nectaries or potentially homologous basal intercarpellary nectaries (0) absent, (1) present.

113 Number of ovules per carpel (0) one, (1) two or varying between one and two, (2) more than two.

114 Placentation (0) ventral, (1) laminar-diffuse or “dorsal.” Described as ventral by Friis et al. (2015) based on the relation of the ovule to the bract, but the bract shows the orientation of the carpel relative to the inflorescence axis, not to the floral axis, which is unknown. We scored living Chloranthaceae and Ceratophyllum as ventral, based on development (Endress & Doyle, 2009), but potentially related fossils as unknown.

115 Ovule direction (0) pendent, (1) horizontal, (2) ascendent.

116 Ovule curvature (0) anatropous (or nearly so), (1) orthotropous (including hemitropous).

117 Integuments (0) two, (1) one.

118 Outer integument shape (0) semiannular, (1) annular. Orthotropous taxa are scored as unknown.

119 Outer integument lobation (0) unlobed, (1) lobed.

120 Outer integument thickness (at middle of integument length) (0) two cells, (1) two and three to four, (2) four and five, or more; ordered. Friis et al. (2015, p. 199) stated that there may be only two cell layers, but that this is uncertain because it is difficult to distinguish the exotesta from the fruit wall and because there may be additional cells above holes in the endotesta (see Friis et al., 2015, fig. 14). Based on the latter, we score Canrightiopsis as 1.

121 Inner integument thickness (0) two cells, (1) two and three, or three, (2) three and more. Friis et al. (2015) described Canrightiopsis as having “several” layers of thin-walled cells, which are often collapsed, but their fig. 14 shows three cell layers; because we consider the state uncertain, we score Canrightiopsis as 1/2.

122 Chalaza (0) unextended, (1) pachychalazal, (2) perichalazal. Orthotropous taxa scored as unknown.

123 Nucellus (0) crassinucellar (including weakly so), (1) tenuinucellar or pseudocrassinucellar.

124 Fruit wall (0) wholly or partly fleshy, (1) dry.

125 Lignified endocarp (0) absent, (1) present. Scored only in fleshy fruits.

126 Fruit dehiscence (0) indehiscent or dehiscing irregularly, dorsally only, or laterally, (1) dehiscent ventrally or both ventrally and dorsally, (2) horizontally dehiscent with vertical extensions.

127 Hooked hairs on fruit (0) absent, (1) present.

128 Testa (0) slightly or non-multiplicative, (1) multiplicative. Because this character is defined by comparison with the number of cell layers in the ovule stage, it is not applicable in fossils.

129 Exotesta (0) unspecialized, (1) palisade or shorter sclerotic cells, (2) tabular, (3) longitudinally elongated, more or less lignified cells.

130 Mesotesta lignification (0) unlignified, (1) with sclerotic layer, (2) with fibrous layer. Characters 130 and 131 are scored as unknown (inapplicable) in taxa with a two-layered outer integument.

131 Mesotesta fleshiness (0) not juicy, (1) wholly or partly modified into a juicy sarcotesta.

132 Endotesta (0) unspecialized, (1) single layer of thin-walled cells with fibrous endoreticulum, (2) multiple layer of thin-walled cells with fibrous endoreticulum, (3) tracheidal, (4) palisade of thick-walled cells.

133 Tegmen (0) unspecialized, (1) thick-walled exo- and endotegmen, (2) fibrous to sclerotic exotegmen.

134 Ruminations (0) absent, (1) testal, (2) tegminal and/or chalazal.

135 Operculum (0) absent, (1) present.

136 Aril (0) absent, (1) present.

137 Female gametophyte (0) four-nucleate, (1) eight- or nine-nucleate.

138 Endosperm development (0) cellular, (1) nuclear, (2) helobial.

139 Endosperm in mature seed (0) present, (1) absent. Characters 139 and 141 are clearly visible with synchrotron radiation X-ray tomographic micrography.

140 Perisperm (0) absent, (1) from nucellar ground tissue, (2) from nucellar epidermis.

141 Embryo (0) minute (less than 1/2 length of seed interior), (1) large.

142 Cotyledons (0) two, (1) one.

143 Germination (0) epigeal, (1) hypogeal.

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Doyle, J.A., Endress, P.K. Phylogenetic Analyses of Cretaceous Fossils Related to Chloranthaceae and their Evolutionary Implications. Bot. Rev. 84, 156–202 (2018). https://doi.org/10.1007/s12229-018-9197-6

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