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Abstract—A fossil from the Early Eocene London Clay flora of southern England ... Its Early Eocene age might seem to contradict molecular evidence that ...
Systematic Botany (2008), 33(4): pp. 636–646 © Copyright 2008 by the American Society of Plant Taxonomists

A Seed Related to Myristicaceae in the Early Eocene of Southern England James A. Doyle,1 Steven R. Manchester,2 and Hervé Sauquet3 1

Department of Evolution and Ecology, University of California, Davis, California 95616 U.S.A. ([email protected]) 2 Florida Museum of Natural History, Gainesville, Florida 23611-7800 U.S.A. ([email protected]) 3 Jodrell Laboratory, Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3DS, U.K. ([email protected]) Communicating Editor: James F. Smith Abstract—A fossil from the Early Eocene London Clay flora of southern England provides the earliest confirmed seed record of Myristicaceae (Magnoliales). The specimen, which was fractured transversely to show internal structure, reveals prominent longitudinal ruminations of the kind found today only in the Myristicaceae. We describe this fossil as Myristicacarpum chandlerae sp. nov. and discuss its phylogenetic and biogeographic implications. Its Early Eocene age might seem to contradict molecular evidence that Myristicaceae diversified in the Miocene, but this depends on whether it belongs in the crown group of the family or on the stem lineage leading to it. To address this question, we review the distribution of ruminations, aril type, and seed size and shape on a molecular and morphological phylogeny of extant Myristicaceae. Myristicacarpum chandlerae resembles some extant genera and not others in presence of ruminations, small size, and elongate shape, but these characters are highly homoplastic in living Myristicaceae and are equally consistent with a position in the crown group or on the stem lineage. However, biogeographic arguments favor a pre-Miocene age for the crown group. Myristicaceae join a growing list of taxa in which modern-appearing fossils predate ages inferred from molecular divergences. Keywords—biogeography, London Clay, Myristicaceae, paleobotany, seed morphology, Tertiary.

Myristicaceae, which consist of 21 genera and nearly 500 species, including the cultivated nutmeg Myristica fragrans, are a medium-sized family of angiosperm trees with a pantropical distribution, largely confined to lowland rainforest habitats. Along with Annonaceae, Magnoliaceae, and three monogeneric families (Degeneriaceae = Degeneria, Eupomatiaceae = Eupomatia, and Himantandraceae = Galbulimima), they belong to Magnoliales (sensu APG 1998; APG II 2003), one of four orders in the magnoliid clade (Magnoliidae sensu Cantino et al. 2007), which also includes Laurales, Canellales, and Piperales. Fruits of Myristicaceae are unilocular and berry-like but often dehiscent along the ventral suture, with a single seed that typically exhibits a prominent aril and distinctly ruminate endosperm in cross section. This combination of characters would seem to facilitate recognition of Myristicaceae in the fossil fruit and seed record. However, as discussed by Doyle et al. (2004), the fossil record of this family has proven to be unusually elusive compared to that of other relatively large woody magnoliid families, notably Magnoliaceae, Annonaceae, and Lauraceae. The contrast with Annonaceae merits particular attention. Doyle et al. (2004) argued that phylogenetic relationships and geographic distributions in Annonaceae and Myristicaceae would suggest that both families began to radiate in Africa and South America and later dispersed into Asia. In terms of timing, this would suggest an origin in the Late Cretaceous, when the South Atlantic was much narrower than today, and dispersal to Asia in the Tertiary, when Africa and Eurasia converged (Doyle and Le Thomas 1997). This scenario was consistent with analyses of molecular divergences within Annonaceae, which dated the crown group (the most recent common ancestor of all living members and its derivatives) as Late Cretaceous or Paleocene (57–82 MY), and the presence of annonaceous seeds in the Late Cretaceous (Maastrichtian) of Africa (Chesters 1955), the Paleocene of Pakistan (Tiffney and McClammer 1988) and the Eocene of England (Reid and Chandler 1933) and North America (Manchester 1994). However, there is much less molecular divergence among extant genera of the Myristicaceae than in Annonaceae, and estimates of the

crown group age are consequently younger, namely Miocene (15–21 MY), when the South Atlantic was nearly as wide as it is today. This could mean either that Myristicaceae are much younger than Annonaceae and attained their present distribution by long-distance dispersal across the South Atlantic Ocean, or that molecular evolution slowed drastically in Myristicaceae, resulting in incorrect molecular age estimates. Doyle et al. (2004) noted that “If Myristicaceae had a history similar to that of Annonaceae, their seeds would be expected in the London Clay, but none has been recognized (Reid and Chandler 1933; Chandler 1961; Collinson and Cleal 2001).” Indeed, the diverse assemblage of well preserved pyritized seeds from the Lower Eocene London Clay Formation of southern England is rich in thermophilic taxa, including Nypa, Annonaceae, Lauraceae, Icacinaceae, and Menispermaceae. Myristicaceous seeds have been described from the Miocene of Germany (Gregor 1977), but there are few if any convincing reports of the family from the Early Tertiary and none from the Cretaceous. This would be consistent with molecular evidence for a surprisingly late diversification of the family (Doyle et al. 2004), or it could be due to some unexplained bias against its preservation or recognition in the fossil record. While reexamining fossil plants in the collections from the London Clay flora with these questions in mind, we recognized a previously unassigned seed that shows clear affinities with Myristicaceae. This occurrence is significantly older than the next convincing record of the family, Myristicacarpum miocaenicum from the Middle Miocene of Germany (Gregor 1977), based on lignitized seeds with ruminations of the myristicaceous type and dehiscent pericarps. In this paper, we place this fossil on record as the earliest confirmed seed occurrence of Myristicaceae, predated only by a report of myristicaceous wood from the Paleocene of the Sahara (Boureau 1950), and discuss its likely relationships in the context of the recent phylogenetic analysis of Magnoliales and Myristicaceae by Sauquet et al. (2003; Fig. 1). Furthermore, we examine the implications of this and previously described fossils for insights into the timing of the radiation of the family and its biogeographic history. This examination 636

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FIG. 1. Parsimony optimization of the seed rumination character in extant Myristicaceae and outgroups, based on relationships found in a combined molecular and morphological phylogenetic analysis (Sauquet et al. 2003). The schematic drawings represent seeds in longitudinal section (testa in black, tegmen in gray, endosperm in white). Abbreviations: Pycn = pycnanthoids, Broch = Brochoneura, Maul = Mauloutchia.

leads us to consider general principles involved in relating fossils to living taxa and molecular age estimates. MATERIALS

AND

METHODS

The specimen described and illustrated by Chandler (1961) as an unnamed species, Carpolithus sp., was reexamined and photographed in the paleobotanical collections of the Natural History Museum (BM), London. The Herne Bay locality, from which the specimen was collected, yields pyritized fruit and seed fossils liberated from the London Clay beds by modern erosion and wave action (Reid and Chandler 1933; Chandler 1961; Collinson and Cleal 2001). Chandler (1961) fractured the specimen transversely to reveal internal structure of the seed, but her published photograph of the cross section was too dark to show the details clearly. We provide new images of the same specimen under greater magnification to more clearly document its morphology, which in fact was accurately portrayed in the written description and diagram provided by Chandler (1961, p. 316). Data on presence and absence of endosperm ruminations and an aril in extant Myristicaceae (Table 1) are taken from Sauquet et al. (2003). Data on seed dimensions were compiled from the literature and our observations of herbarium material at Berkeley (UC) and the Natural History Museum, London (BM) (Table 2). In four cases, we have provided different measures from different sources for the same species. When authors gave a range of measures for a given species, we have given the average of the two extremes in Table 2 and the corresponding graphs. We used MacClade (Maddison and Maddison 2001) to reconstruct character evolution on trees based on parsimony and to evaluate the relative parsimony of alternative positions for M. chandlerae.

TAXONOMIC TREATMENT MYRISTICACARPUM Gregor, 1977. Paläontologische Zeitschrift 51: 203.—TYPE SPECIES: Myristicacarpum miocaenicum Gregor, 1977. Myristicacarpum chandlerae Manchester, Doyle & Sauquet, sp. nov. (Fig. 2 A–E)—TYPE: ENGLAND. London Clay, Lower Eocene, Herne Bay, BM no. v 30545 (holotype: BM; figured as Carpolithus sp. by Chandler 1961, Pl. 31, Figs. 37, 38 and Text Fig. 51). Seed cast elongate-ellipsoid, rounded basally and apically, length 17.6 mm, equatorial diameter 6 by 4.5 mm (length/ width ratio 2.9:1–3.9:1). Chalaza eccentrically positioned relative to the long axis of the seed. Seed prominently ruminate with irregular longitudinal plate-like intrusions of the seed coat ca 0.1–0.2 mm thick that extend radially inward toward the center of the seed. In transverse section, endosperm seen to be radially dissected and separated to varying depths by the radial plates. Some of the plates extend to the center where they merge with one another axially to form V-shapes, but between the deeper plates are some shorter ones that subdivide the wedges of endosperm produced by the deeper plates. Seed surface with conspicuous, longitudinal, finely

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TABLE 1. Seed rumination and aril characters in extant Myristicaceae. Data are extracted from the morphological matrix of Sauquet et al. (2003; characters 107 and 108, respectively) and were compiled from Corner (1976), Sinclair (1958), Capuron (1973), Takhtajan (1988), Wilde (2000), and personal observations by H. S. on most of the genera (see also Sauquet 2004). Full species names are given for the monotypic genera. Genus

Ruminations

Aril

Bicuiba oleifera Brochoneura Cephalosphaera usambarensis Coelocaryon Compsoneura Doyleanthus arillata Endocomia Gymnacranthera Haematodendron glabrum Horsfieldia Iryanthera Knema Mauloutchia Myristica Osteophloeum Otoba Paramyristica sepicana Pycnanthus Scyphocephalium Staudtia kamerunensis Virola

present absent absent present absent ? present present present present absent present absent present absent present present present present absent present

entire rudimentary deeply laciniate deeply laciniate entire deeply laciniate entire/deeply laciniate deeply laciniate absent entire entire entire rudimentary/deeply laciniate deeply laciniate entire deeply laciniate deeply laciniate deeply laciniate entire entire deeply laciniate

crenulate and sinuous surface ridges reflecting the internal rumination pattern. Derivation of Specific Epithet—This species is named in honor of M. E. J. Chandler, coauthor of the monumental London Clay flora, who previously figured and described the specimen. Remarks—The genus Myristicacarpum was established by Gregor (1977) based on seven lignitized fruits and seeds from the Middle Miocene of Germany. It accommodates fossil fruits and seeds with “general structure similar to that of Myristicaceae, namely two-valved berries with leathery pericarp, three-layered testa, anatropous ovule, and ruminate endosperm. Aril probably hardly or not at all laciniate” (translated). Several of the diagnostic characters of Myristicacarpum are not preserved in M. chandlerae, notably those of the fruit wall and aril. However, those characters that are preserved, in particular the characteristic V-shaped ruminations intruding into the seed, are so similar to those of M. miocaenicum and living Myristicaceae that we prefer to treat the fossil as a new species of Myristicacarpum rather than erect a new genus. Myristicacarpum chandlerae is similar to M. miocaenicum in its rumination pattern and length but differs in its much narrower width (4.5–6 mm vs. 13–16 mm) and consequently more elongate shape. DISCUSSION Relation of the Fossil to Myristicaceae—In her initial treatment of this fossil, Chandler stated “the relationship of this species is not known but its distinctive appearance should make it readily recognizable if comparable material were available.” Now that comparisons have been extended to include Myristicaceae the affinities become clear. The presence of ruminate endosperm and the pattern of rumination are particularly useful for resolving its affinities. Corrugations or invaginations of one or both seed coat

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layers (tegmen, testa) give rise to ruminate endosperm in various families of angiosperms, including Annonaceae, Myristicacaeae, Eupomatiaceae, Degeneriaceae, Canellaceae (Cinnamosma), Menispermaceae (tribe Anomospermeae), Oxalidaceae, and Vitaceae, and to ruminate cotyledonary tissue in exalbuminous seeds such as those of Hernandiaceae (Corner 1976). Ruminate endosperm occurs in at least 58 families and is scattered phylogenetically (Bayer and Appel 1996). However, the patterns of rumination differ greatly, complementing other morphological features of the seed to provide useful characters for systematic assessment and identification. The seed coat in Myristica and other ruminate genera of the family intrudes in the form of irregularly sinuous, longitudinally oriented discontinuous plates that extend radially inward nearly to the center of the seed (Fig. 2; Warburg 1897; Uphof 1959). When viewed transversely, it can be seen that plates arising from the same side of the seed closely approach each other or sometimes converge near the center of the seed to form V-shaped patterns. This pattern of radially oriented irregular longitudinal plates differs from that of other Magnoliales. Annonaceae have perichalazal seeds, in which the raphe runs around the seed as a result of differential basal growth. Their ruminations form thick and irregular but mainly transverse or radial plates and pegs (in the phylogenetically basal lines), a bisymmetrical pattern of thin transverse plates, or radial spines (van Setten and Koek-Noorman 1992; Doyle and Le Thomas 1996; Doyle et al. 2000, 2004). Another basal angiosperm, Austrobaileya (Austrobaileyales), has ruminate perichalazal seeds that are readily distinguished by more highly ramified ruminations (Endress 1980). Degeneria and Eupomatia, which, like Myristicaceae, are not perichalazal, have irregular ruminations of the type found in basal Annonaceae; similar but more reduced ruminations have been reported in Galbulimima (= Himantandraceae; Doweld and Shevyryova 1998). Ruminations of Myristicaceae also differ in development from those of other Magnoliales and Austrobaileya, which arise by ingrowth of both the outer integument (testa) and the inner integument (tegmen) and are thus described as testal (Corner 1976; Takhtajan 1988). In Myristicaceae, where seed development has been studied in Horsfieldia, Knema, and Myristica, the ruminations have been variously interpreted as derived from the chalaza, the inner integument, or both (Periasamy 1962; Mohana Rao 1974; Corner 1976, 1983; Van Heel 1982; Takhtajan 1988). In Horsfieldia and Knema, Van Heel (1982) showed that the region where the inner integument joins the nucellus enlarges greatly during seed development, and ruminations form as finger-like intrusions of the intercalated chalazal tissue. Corner (1983) confirmed this interpretation of the seeds studied by Van Heel, but he suggested that ruminations may be partly derived from the free part of the tegmen in another Knema species. Seeds of other taxa with ruminate endosperm, e.g. among monocots and eudicots, are readily distinguished from those of Myristicaceae in terms of shape, symmetry, the relative positions of the micropyle, hilum, chalaza, and raphe (when present), and the pattern and depth of seed coat intrusions into the endosperm. Often in these taxa the rumination is only superficial, corresponding to shallow intrusions of the seed coat (e.g. Passifloraceae; Corner 1976). Seeds of many palms have deeply ruminate endosperm with a pattern strikingly similar to that of Myristicaceae, with blade-like intru-

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TABLE 2. Measurements of seed size (average or midpoint of range) and shape (our measurements usually based on single specimens, except N = 13 for Myristica fragrans; number of specimens not indicated in literature references). For documentation of synonymy, see Sauquet et al. (2003). SRM = measurements by S. R. Manchester of specimens at UC (except Myristica fragrans). 1. UC specimen identified as Horsfieldia macrocoma. 2. UC specimen identified as Pycnanthus kombo. 3. Material described by Warburg (1897) as Pycnanthus kombo. 4. Material described by Warburg (1897) as Pycnanthus schweinfurthii. 5. UC specimen identified as Staudtia stipitata. 6. Material described by Warburg (1904) as Staudtia gabonensis. 7. UC specimen identified as Knema venosa. Taxon

L × W (mm)

L/W

Source of measurements

Bicuiba oleifera (Schott) W.J. de Wilde Brochoneura acuminata (Lam.) Warb. Brochoneura madagascariensis (Lam.) Warb. Brochoneura vouri (Baill.) Warb. Cephalosphaera usambarensis (Warb.) Warb. Coelocaryon preussii Warb. Coelocaryon preussii Warb. Compsoneura debilis (A. DC.) Warb. Compsoneura sprucei (A. DC.) Warb. Compsoneura mutisii A.C. Sm. Compsoneura capitellata (A. DC.) Warb. Doyleanthus arillata Capuron ex Sauquet Endocomia macrocoma (Miq.) W.J. de Wilde1 Endocomia canarioides (King) W.J. de Wilde Gymnacranthera paniculata (A. DC.) Warb. Haematodendron glabrum Capuron Horsfieldia brachiata (King) Warb. Horsfieldia irya (Gaertn.) Warb. Horsfieldia lancifolia W.J. de Wilde Horsfieldia valida (Miq.) Warb. Iryanthera lancifolia Ducke Iryanthera hostmannii (Benth.) Warb. Knema glauca (Blume) Warb. Knema intermedia (Blume) Warb. Knema kinabaluensis J. Sinclair Knema oblongifolia (King) Warb. Mauloutchia chapelieri (Baill.) Warb. Mauloutchia echinocarpa Capuron ex Sauquet Mauloutchia heckelii Capuron emend. Sauquet Mauloutchia humblotii (H. Perrier) Capuron Mauloutchia rarabe (H. Perrier) Capuron Mauloutchia sambiranensis (Capuron) Sauquet Myristica chartacea Gillespie Myristica fragrans Houtt. Myristica hollrungii Warb. Myristica hypargyraea A. Gray Osteophloeum platyspermum (A. DC.) Warb. Otoba novogranatensis Moldenke Otoba novogranatensis Moldenke Paramyristica sepicana (Foreman) W.J. de Wilde Pycnanthus angolensis (Welw.) Warb.2 Pycnanthus angolensis (Welw.) Warb.3 Pycnanthus angolensis (Welw.) Warb.4 Scyphocephalium chrysothrix Warb. Staudtia kamerunensis Warb.5 Staudtia kamerunensis Warb.6 Staudtia kamerunensis Warb. Virola calophylla Warb. Virola elongata (Benth.) Warb. Virola koschnyi Warb. Virola venosa (Benth.) Warb.7

21 × 14 20 × 13 22.5 × 22.5 × 20 25 × 17 × 14 47.5 × 29 23 × 12 30 × 15 13 × 7 25 × 16 28 × 22 40 × 30 22 28 × 12 52 × 23.5 18 × 15 21.5 × 18 25 × 23 19 × 19 16 × 16 19 × 32 18 × 30 12 × 22 19 × 13 30 × 15 34 × 16 16 × 16 27 × 24 × 21 15 35 × 35 × 27 30 × 20 × 19 25 × 25 17.5 20 × 13 23 × 17 19 × 11 32 × 22 8 × 18 18 × 15 22 × 25 30 × 15 14 × 10 20.5 × 12.5 22.5 × 13.5 22.5 × 35 23 × 13 20 × 12 35 × 15 15 × 9 10 × 8 17 × 12 11 × 10

1.50 1.54 1.19 1.61 1.64 1.92 2.00 1.86 1.56 1.27 1.33

Wilde (1991) Capuron (1973) Capuron (1973) Capuron (1973) Verdcourt (1997) SRM (Toussaint 2422) Warburg (1897) Warburg (1897) SRM (P. H. Allen 6009) SRM (Gutierrez 35648) SRM (Ducke 1486) Sauquet (2003) SRM (M. Ramos 43273) Wilde (1991) SRM (M. Ramos 41102) Capuron (1972) SRM (Elmer 21338) SRM (Arndja 94) SRM (E. F. Vogel 5267) SRM (Clemens 26971) SRM (Ducke 1492) Warburg (1897) SRM (M. Ramos, G. Edaño 49851) SRM (Foxworthy 12121) SRM (Clemens 29358, 26697A) SRM (Chew Wee-Lek 885) Capuron (1973) Sauquet (2004) Capuron (1973) Capuron (1973) Perrier de la Bâthie (1952) Sauquet (2004) SRM (A. C. Smith 501) SRM (UF modern ref. coll. 1231) SRM (Clemens 10511) SRM (Satchell 342) Warburg (1897) SRM (A. Gentry 12009) Warburg (1897) Wilde (1991) SRM (Gilbert 3764) Warburg (1897) Warburg (1897) Warburg (1897) SRM (Wagemans 2049) Warburg (1904) Warburg (1897) SRM (Krukoff 5492) SRM (Krukoff 1590) SRM (Gentle 9105) SRM (Ducke 1304)

sions of the seed coat extending 1/3 or more of the distance across the seed as seen in transverse section (Uhl and Dransfield 1987). In tangential view, however, the seed coat intrusions in Arecaceae are usually arrayed in a closed reticulate pattern with areoles that lack well-defined orientation (cf. images of Beccariophoenix, Heterospathe, Kerriodoxa, Raphia, Phoenicophorium, Prestoea, and Rhopaloblaste in Uhl and Dransfield 1987). In contrast, in Myristicaceae the ruminations form a more open reticulum and (at least in those specimens that we have examined closely) have a predominantly longitudi-

2.33 2.21 1.20 1.19 1.09 1.00 1.00 0.59 0.60 0.55 1.46 2.00 2.13 1.00 1.20 1.13 1.54 1.00 1.54 1.35 1.73 1.45 0.44 1.20 0.88 2.00 1.40 1.64 1.67 0.64 1.77 1.67 2.33 1.67 1.25 1.42 1.10

nal orientation (see Myristicacarpum chandlerae in Fig. 2A and Myristica fragrans in Fig. 2J). The ruminations in M. chandlerae are indistinguishable from those observed in extant members of the Myristicaceae that have ruminate seeds (Fig. 2; Table 1). In their rumination character, Sauquet et al. (2003) treated the tegminal-chalazal ruminations of Myristicaceae as a separate state from the testal ruminations of other Magnoliales. With the relationships found by Sauquet et al. (Fig. 1), and with ruminations absent in both Magnoliaceae and Laurales, the sister group of

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FIG. 2. Seeds of Myristicacarpum chandlerae sp. nov. and selected extant species of Myristicaceae for comparison, scale bars calibrated in mm. A-E. Holotype of M. chandlerae, BM v 30545, Eocene London Clay flora, Herne Bay, southern England. A. Longitudinal view showing longitudinal grooves corresponding to infolds of the seed coat. Transverse crack indicates level of the cross section shown in D and E. B. Apical view. C. Basal view. D. Cross section showing ruminate endosperm. E. Detail of cross section, showing radially oriented plates of seed coat intruding the endosperm. F, G. Knema kinabaluensis J. Sinclair, UC 557347; J. & M. S. Clemens 26697. Fruit in lateral view and cross section. H, I. Horsfieldia brachiata (King) Warb. var. sumatrana (Miq.) J. Sinclair, UC 289992; E. D. Merrill 21338, Borneo, fruit in lateral view and cross section. J-L. Myristica fragrans Houtt., UF modern ref. coll. 434 (commercial nutmeg).

Magnoliales, it is most parsimonious to assume the two sorts of ruminations evolved independently in Myristicaceae and the common ancestor of Annonaceae, Eupomatia, Degeneria, and Galbulimima. If this is correct, the longitudinal ruminations indicate that M. chandlerae is more closely related to Myristicaceae than it is to any other group. If ruminations of all these groups are treated as the same state, there are two equally parsimonious scenarios: either ruminations evolved independently in Myristicaceae and other Magnoliales, or they arose once in the common ancestor of Magnoliales and were lost in Magnoliaceae. The different development of the two types could then be taken as support for the former

scenario. Other features of the seed, e.g. lack of the perichalazal condition, the thickness and spacing of the tegminal plates, and the position of the chalaza somewhat offset from the seed’s axis of symmetry, are also consistent with a relationship to Myristicaceae. Stem or Crown—It is desirable to consider whether M. chandlerae is a member of the crown group of Myristicaceae or a stem relative (i.e. on the stem lineage leading to the extant clade, or a branch attached to it). This question has important implications for biogeographic history and for comparison of paleobotanical data with molecular age estimates, which apply only to crown groups (Doyle and Dono-

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ghue 1993; Fig. 3). In general, if a fossil (X) has at least one apomorphy (A) shared by all living members of the group but is more plesiomorphic in another character (B), it can be placed on the stem lineage. Because such fossils are usually extinct side lines rather than direct ancestors of the crown clade, they may be either older or younger than the crown group. If a fossil (Y) has derived states of the crown group as a whole in its preserved characters (A and B), plus at least one derived feature of a subgroup of the crown group (C), it can be placed in the crown group, and its age can be used as a minimum age of the crown group node. However, the situation is less clear when a fossil (Z) has derived states of the crown group as a whole in its preserved characters (A and B) but no apomorphies of any subgroup (C). It is tempting to assume such a fossil belongs in the crown group, but it could be on the stem lineage, between the point where the last preserved synapomorphy (B) evolved and the crown group node. Depending on whether the preserved synapomorphies originated late or early in the history of the stem lineage, the first plant with these features could be close to the crown group in age or much older. Such a plant, although unambiguously related to the modern clade, might not look very modern: it might lack many crown-group advances in other organs that evolved later (D and E). As discussed further below, this situation is far from hypothetical, as there are several recently described fossils that resemble living clades in all their preserved characters but are much older than molecular age estimates. To address the systematic position of M. chandlerae relative to crown-group Myristicaceae, we next consider the distribution of those seed characters that vary within the family (Tables 1, 2) in the context of the phylogenetic relationships among modern Myristicaceae inferred by Sauquet et al. (2003). One of the most conspicuous variable characters is endosperm rumination. The vast majority of Myristicaceae have ruminate seeds. However, notable exceptions are three American genera (Compsoneura, Iryanthera, and Osteophloeum) and the genera of the Afro-Malagasy clade that Sauquet et al. (2003) designated the mauloutchioids (Table 1). Current un-

FIG. 3. Placement of fossils (X, Y, Z) in the crown group and on the stem lineage leading to it in relation to the possession of apomorphies (A, B, C). See text for discussion.

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derstanding of phylogenetic relationships within Myristicaceae leaves the parsimony optimization of this character equivocal (Fig. 1). Either ruminations appeared once in the common ancestor of all extant members and were secondarily lost in the taxa listed above, or ruminations were ancestrally absent in the family and evolved at least twice independently. It may seem more likely that such a distinctive morphology only evolved once, but the second alternative cannot be ruled out. Recent genera of Myristicaceae also vary in presence vs. absence and degree of dissection of an aril (Table 1). Optimization of this character on the tree of Sauquet et al. (2003, Fig. 14) indicates that a deeply laciniate aril is ancestral in Myristicaceae and a synapomorphy of the family. The aril became entire or only apically laciniate in Staudtia and one or more times within the myristicoid clade (Compsoneura, Horsfieldia, Knema, and Scyphocephalium). It was reduced to the rudimentary type within the mauloutchioid clade and completely lost in the myristicoid genus Haematodendron. Unfortunately, because M. chandlerae is preserved as an infilling of the inside of the seed coat, we cannot determine whether or not it had an aril, but this character may be valuable in evaluating the affinities of other fossils. Two other potentially informative features of M. chandlerae are its relatively small size (ca. 18 mm) and elongate shape (L/W ca. 3). Both seed size and seed shape vary greatly across extant Myristicaceae (Table 2), and even within some genera, but dimensions within species are generally more consistent (an exception is cultivated nutmeg, Myristica fragrans, in which most commercial seeds that we have measured vary between 18 × 14 mm and 28 × 18 mm but rare specimens range up to 36 × 12 mm). The continuous nature of these characters and their high variation within taxa make them problematic for cladistic purposes, and partly for this reason they were not used by Sauquet et al. (2003), but it should not be assumed a priori that they are systematically worthless. Literature data on seed dimensions vary greatly in quality (for example, it is often unclear whether mean or maximum dimensions are being given, and often measures are given only to the nearest half centimeter), and a proper biometric study would be desirable. However, the data in Table 2 may be sufficient for a preliminary assessment. Figure 4 presents maximum seed dimension (usually length, but width in the few taxa with oblate seeds) for various numbers of species in all 21 genera of Myristicaceae, summarized in a histogram. To estimate the ancestral seed size, it would be desirable to break these measures into discrete states based on gaps in the size distribution and plot them on a cladogram. There are no obvious gaps in the distribution in Fig. 4, except around 26 mm, which many genera cross. However, there are several genera in which observed average sizes do not range below 20 mm and others in which they are consistently less than 20 mm. We therefore used 20 mm as a limit between states (0 = less than 20 mm, 1 = 20 mm or more), scored genera that cross this limit as uncertain (i.e. 0/1), and plotted the character on cladograms. If seed size is plotted on a cladogram of Myristicaceae alone (not shown), the inferred ancestral state is 20 mm or larger, with smaller seeds derived 9–11 times (including origins within genera). This result would suggest that M. chandlerae is in the crown group, related to one or another of the small-seeded lines. However, most of the outgroups of Myristicaceae (other magnoliids) have small seeds, except some

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FIG. 4. Seed size (maximum dimension) in species of all 21 genera of extant Myristicaceae (mm). Data from Table 2. Histogram shows numbers of species (or in four cases measures of the same species by different authors) in each size category.

but not all basal members of the Calycanthaceae (Idiospermum; Cooper and Cooper 2004), Lauraceae (Hypodaphnis, Beilschmiedia, Cryptocarya, and Endiandra; Kostermans 1950, 1957; Fouilloy 1965; Cooper and Cooper 2004; Rohwer and Rudolph 2005), and Hernandiaceae (Kubitzki 1969), which were therefore scored as uncertain (0/1). When outgroups are included (Fig. 5), the ancestral seed size in Myristicaceae becomes equivocal, implying that M. chandlerae could be either in the crown group or on the stem lineage. The same result is obtained with seed volume, estimated by treating seed shape as an ellipsoid (not shown). Figure 6 shows a similar plot of length vs. width. Again there is much variation within genera, and the clearest break is between a few oblate genera (Iryanthera, Osteophloeum, Scyphocephalium) and the remaining taxa, at about 0.8. However, there is a somewhat lower point in the distribution among more elongate taxa, at about 1.9. We therefore defined shape as an ordered three-state character, with one limit between states at 0.8 and another at 1.9 (0 = less than 0.8, 1 = 0.8–1.9, 2 = more than 1.9). The L/W ratio for M. chandlerae is higher than any of the average values for living species in Fig. 6; unfortunately, with only one fossil specimen there is no way to know whether this shape was typical for the species or an extreme in its intraspecific variation. We did not

score outgroups for this character because of the questionable comparability of shape variation in the unusual pachychalazal seeds of Myristicaceae with that in non-pachychalazal taxa. Optimization of this character on the cladogram (Fig. 7) indicates that nearly spherical to moderately elongate seeds (L/W 0.8–1.9) are ancestral and both oblate and highly elongate seeds are derived, with the latter originating at least five times within Myristicaceae. Seed shape might therefore support the view that M. chandlerae belongs in the crown group, related to one or another of the taxa with elongate seeds (Coelocaryon, Endocomia, Knema, Paramyristica, or Staudtia). This inference does not hold up when the potentially informative characters of M. chandlerae are considered in combination. For this purpose, we added the fossil to the Sauquet et al. (2003) data set (scored as having tegminal ruminations, size < 20 mm, L/W > 1.9) and determined the parsimony scores of all its possible positions on the cladogram (with outgroups included). This revealed 10 most parsimonious positions for M. chandlerae, including one on the stem lineage and nine within Myristicaceae (indicated by arrows in Fig. 7). The high level of homoplasy in seed dimensions, the intraspecific variation we observed in Myristica fragrans, and doubts regarding the accuracy of published measurements in

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FIG. 5. Cladogram of extant Myristicaceae and outgroups based on molecular and morphological data (Sauquet et al. 2003), showing inferred evolution of seed size, with a break between states at 20 mm (based on Fig. 4, with taxa that cross the limit between states scored as uncertain, i.e. 0/1). Abbreviations as in Fig. 1.

extant taxa are reasons for caution in utilizing these characters. However, better molecular resolution of relationships, especially in the myristicoid clade, could resolve whether ruminations were ancestral or derived within the family, while a more sophisticated biometric analysis and closer examination of other aspects of seed morphology might pro-

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vide more useful phylogenetic data. Discovery of more specimens of M. chandlerae might also indicate whether or not it had an aril and clarify whether the highly elongate shape of the present specimen was typical of the species. Several authors have argued for restricting familiar names of extant taxa such as Myristicaceae to the respective crown group (de Queiroz and Gauthier 1992; Doyle and Donoghue 1993; Cantino et al. 2007). This practice circumvents the problem that broader usages may include fossil stem relatives that differed from the crown group in biologically important respects, and it has the advantage of equating familiar names with clades recognized in molecular analyses, which include only extant taxa. If Myristicaceae are defined in this way, then M. chandlerae cannot be assigned unequivocally to the family, because it remains uncertain whether the fossil belongs in the crown group. However, based on its tegminal ruminations and other characters, we are confident that it is more closely related to Myristicaceae than it is to any other crown clade. In other words, it can be assigned to the stembased clade (= total clade) that includes living Myristicaceae. Following Cantino et al. (2007), this clade could be designated by adding the prefix “Pan-” to the name of the extant clade. Thus M. chandlerae could be assigned to “PanMyristicaceae” whether or not it belongs to Myristicaceae in a strict crown group sense. We emphasize that such a name would in no way favor a position on the stem lineage over one in the crown group. Other Reports of Myristicaceae in the Fossil Record— Berry (1924) described putative seed and fruit casts from the Late Eocene of Texas as Myristica catahoulensis. These fossils have grooves that superficially resemble myristicaceous ru-

FIG. 6. Seed shape (length/width) in species of 20 of 21 genera of extant Myristicaceae. Data from Table 2. Histograms show numbers of species (or in four cases measures of the same species by different authors) in each shape category. Ovals represent seed shape.

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FIG. 7. Cladogram of extant Myristicaceae based on molecular and morphological data (Sauquet et al. 2003), showing inferred evolution of seed shape, with breaks between states at 0.8 and 1.9 (based on Fig. 6, with taxa that cross the limit between states scored as uncertain, e.g. 0/1). The arrows show all most parsimonious positions of M. chandlerae based on the combination of three characters: ruminations (Fig. 1), seed size (Fig. 5), and the present shape character (with outgroups included). Abbreviations as in Fig. 1.

minations. However, examination of the figured specimen and others at USNM from the same locality that are more completely preserved indicates that they are molds of an endocarp of Mastixiaceae (Cornales). Another report of seeds of the family was that of Virola tertiaria Berry (1929) from the Oligocene of Belen, Peru. The fossil has external morphology consistent with a myristicaceous seed, but the specimen that was broken transversely (reexamined at USNM) does not show the ruminations that would provide more positive evidence for the identification. The type species of Myristicacarpum (Gregor 1977) is from the Middle Miocene lignites of Schwandorf, Germany. Material of M. miocaenicum Gregor has remains of a dehiscent pericarp and shows spheroidal to ovoid seeds that are 16.5– 18 mm long and 13–16 mm in diameter, with typical myristicaceous ruminations and an entire or hardly laciniate aril. Gregor considered this species to be most similar to Horsfieldia, but also comparable to Knema and Myristica. As discussed above, the presence of ruminations and the size and shape of this fossil do not indicate whether it is a crown-group member or stem relative of Myristicaceae. However, based on the inference of Sauquet et al. (2003) that a deeply laciniate aril was ancestral for Myristicaceae and was modified to an entire or apically laciniate aril in Staudtia and one or more times within the myristicoid clade, the morphology of the aril in M. miocaenicum suggests this fossil belongs in the crown group. Other less conclusive Tertiary reports of Myristicaceae were reviewed by Doyle et al. (2004). These include leaves that resemble those of Myristicaceae but are not clearly distinguishable from other Magnoliales and have not been shown to possess the diagnostic trichome characters of the family. Several dispersed pollen types have been compared with living genera of Myristicaceae, but other possible relationships have not been exhaustively eliminated. Aside from Myristicacarpum, the most convincing record of

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the myristicaceous line, and the oldest record, is a wood type described by Boureau (1950) from the Paleocene of the Sahara as Myristicoxylon princeps. The combination of characters in this wood is indeed most similar to Myristicaceae (E. A. Wheeler, pers. comm.). However, it is not clear whether this fossil was more likely a member of the crown group or a stem relative. In either case, it would be consistent with the view that the crown group originated and began its radiation in Africa (Doyle et al. 2004). Implications for Age and Geographic History of Myristicaceae—With recognition of M. chandlerae in the Early Eocene, Myristicaceae join a growing list of taxa in which crown-group morphology (at least in the plant parts preserved) was attained much earlier than the age of the crown clade inferred from molecular data. Other examples include Winteraceae (Suh et al. 1993; Doyle 2000), Hedyosmum and Chloranthus in the Chloranthaceae (Zhang and Renner 2003; Eklund et al. 2004), and Ephedra (Rydin et al. 2004, 2006). Such cases have sometimes been taken as evidence that the molecular dates are incorrect and the group is much older. This interpretation should not be ruled out, but it is not necessarily correct if the fossils are stem relatives of the corresponding living clades and their derived features originated early on the stem lineage. However, the latter hypothesis leads to the surprising conclusion that the stem lineage maintained a similar morphology for tens of millions of years before radiating into the crown group. We see no reason to reject such a scenario, but if it is correct it poses important evolutionary questions. If the stem lineage was represented by one species through much of its history, what caused its recent radiation? If it underwent a series of earlier radiations and contractions, why did all species die out except the one that gave rise to the crown group? In the case of Myristicaceae, the large number of apomorphies (in addition to tegminal-chalazal ruminations, if these arose on the stem lineage) might be consistent with long existence of the stem lineage; in the data set of Sauquet et al. (2003), these include tanniniferous tubes, sympodially branched trichomes, dioecy, one perianth whorl, fused stamens, loss of filament, sculptured sulcus membrane, one carpel, partially ascidiate carpel form, pachychalazal seed, palisade endotesta, fibrous exotegmen, laciniate aril, and hypogeal germination. On the other hand, if the fossils in question belong to the corresponding crown groups, they suggest that rates of molecular evolution decelerated markedly somewhere on their stem lineages. In such cases molecular dating methods may be misleading, including those that modify the clock assumption to allow for gradual changes in rate of evolution (cf. Anderson et al. 2005; Rydin et al. 2006). An alternative line of reasoning would accept the Miocene molecular age estimate for crown-group Myristicaceae (Doyle et al. 2004) and use it as evidence that M. chandlerae was a stem relative. Under this interpretation, the fact that M. chandlerae has ruminations would be evidence that ruminations were ancestral in Myristicaceae and their absence in the mauloutchioids and the three South American genera was a result of loss. Such arguments have been made, with varying degrees of conviction, for Early Cretaceous relatives of Hedyosmum (Eklund et al. 2004), a Late Cretaceous flower described as related to Victoria in the Nymphaeaceae (Yoo et al. 2005), and Late Cretaceous pollen resembling subgroups of Nothofagus (Cook and Crisp 2005). We believe a better

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understanding of potential errors in molecular dating methods is needed before such arguments can be accepted. The fact that the two Tertiary occurrences that we accept as unequivocally related to Myristicaceae, Myristicacarpum miocaenicum Gregor and M. chandlerae sp. nov., are from Germany and England shows that Myristicaceae or their close relatives formerly occurred in Europe, well outside the current geographic range of the family. This is not surprising from a paleoecological point of view, considering the other thermophilic members of these fossil floras and evidence for warm climatic conditions in the Eocene and Miocene. Because we have not been able to resolve whether M. chandlerae is a stem relative or a crown-group member of Myristicaceae, its bearing on the contrast between Myristicaceae and Annonaceae—that is, that molecular dates for Annonaceae are consistent with a Cretaceous radiation in AfricaSouth America, but not those for Myristicaceae—remains uncertain. If M. chandlerae belongs in the crown group, it would refute the Miocene molecular date for Myristicaceae and suggest that both families may indeed have originated in AfricaSouth America in the Late Cretaceous and dispersed to Laurasia in the Early Tertiary. But if M. chandlerae is a stem relative, the contrast between the two groups would remain, and it would indicate that the line leading to Myristicaceae, or a branch from it, occurred in Laurasia. If so, the crown group might be derived from another line that began to diversify in Africa in the Miocene, as indicated by molecular data, and then reinvaded Eurasia. However, this hypothesis would leave unsolved the problem of transoceanic dispersal of the large seeds of Myristicaceae to South America. For this reason, we consider it most likely that crown-group Myristicaceae are significantly older than the molecular dating implies (cf. Doyle et al. 2004), and that M. chandlerae represents a crown-group lineage that had dispersed from Africa to Eurasia. However, we stress that this is based on biogeographic considerations and cannot be deduced from the morphology of the fossil. Recognition of M. chandlerae in the London Clay raises hope that other seeds related to Myristicaceae await discovery in Lower Tertiary or even older sediments. Discovery of more completely preserved fossils (e.g. including an aril and/or fruit wall), better resolution of phylogenetic relationships among modern Myristicaceae, and more detailed understanding of seed morphology in the extant taxa could further clarify the vexed problem of the age and geographic history of this family. ACKNOWLEDGMENTS. We thank Peta Hayes and Paul Kenrick for access to the London Clay fruit and seed collections at the Natural History Museum, London. JAD wishes to thank Phil Garnock-Jones and the School of Biological Sciences, Victoria University of Wellington for providing facilities and a supportive environment during preparation of this paper. This work was supported in part by NSF grant EAR 0174295 to SRM, and facilitated by support from the NSF Deep Time RCN (RCN0090283).

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