Fossil calibration of Magnoliidae, an ancient lineage of angiosperms

25 Pages·2014·1.56 MB·English

by  Peter Rose

Palaeontologia Electronica
palaeo-electronica.org
Fossil calibration of Magnoliidae,
an ancient lineage of angiosperms
Julien Massoni, James Doyle, and Hervé Sauquet
ABSTRACT
In order to investigate the diversification of angiosperms, an accurate temporal
framework is needed. Molecular dating methods thoroughly calibrated with the fossil
record can provide estimates of this evolutionary time scale. Because of their position
in the phylogenetic tree of angiosperms, Magnoliidae (10,000 species) are of primary
importance for the investigation of the evolutionary history of flowering plants. The rich
fossil record of the group, beginning in the Cretaceous, has a global distribution.
Among the hundred extinct species of Magnoliidae described, several have been
included in phylogenetic analyses alongside extant species, providing reliable calibra-
tion points for molecular dating studies. Until now, few fossils have been used as cali-
bration points of Magnoliidae, and detailed justifications of their phylogenetic position
and absolute age have been lacking. Here, we review the position and ages for 10 fos-
sils of Magnoliidae, selected because of their previous inclusion in phylogenetic analy-
ses of extant and fossil taxa. This study allows us to propose an updated calibration
scheme for dating the evolutionary history of Magnoliidae.
Julien Massoni. Laboratoire Ecologie, Systématique, Evolution, Université Paris-Sud, CNRS UMR 8079,
91405 Orsay, France. [email protected]
James Doyle. Department of Evolution and Ecology, University of California, Davis, CA 95616, USA.
[email protected]
Hervé Sauquet. Laboratoire Ecologie, Systématique, Evolution, Université Paris-Sud, CNRS UMR 8079,
91405 Orsay, France. [email protected]
Keywords: fossil calibration; Canellales; Laurales; Magnoliales; Magnoliidae; Piperales
PE Article Number: 18.1.2FC
Copyright: Palaeontological Association February 2015
Submission: 10 October 2013. Acceptance: 1 July 2014
Massoni, Julien, Doyle, James, and Sauquet, Hervé. 2015. Fossil calibration of Magnoliidae, an ancient lineage of angiosperms.
Palaeontologia Electronica 18.1.2FC; 1-25;
palaeo-electronica.org/content/fc-2
Calibrations published in the Fossil Calibration Series are accessioned into the Fossil Calibration Database
(www.fossilcalibrations.org). The Database is a dynamic tool for finding up-to-date calibrations, and calibration data will be updated
and annotated as interpretations change. In contrast, the Fossil Calibration papers are a permanent published record of the
information on which the calibrations were originally based. Please refer to the Database for the latest data.
MASSONI, DOYLE, & SAUQUET: MAGNOLIIDAE
INTRODUCTION Investigating the evolutionary history of organ-
isms often requires a temporal context, which until
Among the first diverging lineages of angio-
recently was based almost exclusively on the fossil
sperms (outside monocots and eudicots), Magnolii-
record. Insofar as fossils can be placed in a phylo-
dae are the largest clade, comprising about 10,000
genetic tree, a paleontological approach can pro-
species divided among 20 families and four orders:
vide minimum ages and, to a lesser extent,
Magnoliales, Laurales, Canellales, and Piperales
maximum ages for clades. Over the past two
(APG III, 2009). Although Magnoliidae have a
decades, this method has been supplemented with
global distribution extending into the temperate
molecular dating approaches, which generate esti-
zones of both hemispheres, most of their diversity
mates of absolute divergence times throughout the
occurs in tropical areas. This group has been sup-
tree (i.e., not just in the neighborhood of a particu-
ported as monophyletic by the great majority of
lar fossil). The first such studies were based on the
molecular phylogenetic studies (Qiu et al., 1999,
concept of a molecular clock, but the development
2000, 2005, 2006, 2010; Soltis et al., 1999, 2000a,
of new methods has helped to relax the assump-
2000b, 2007, 2011; Mathews and Donoghue,
tion of a strict clock across the tree.
1999, 2000; Savolainen et al., 2000; Graham and
In molecular dating analyses, the fossil record
Olmstead, 2000; Zanis et al., 2002, 2003; Nickrent
provides minimum bounds to calibrate the trees.
et al., 2002; Borsch et al., 2003; Hilu et al., 2003;
These calibration points are not only used to con-
Jansen et al., 2007; Moore et al., 2007, 2010; Bur-
vert the time scale of relative ages into one of
leigh et al., 2009). Although the majority of the rela-
absolute ages, but they also serve as anchors for
tionships among families of Magnoliidae are well
modeling molecular rate variation across the tree
established, the exact positions of Hydnoraceae
(e.g., Sanderson, 1997; Sauquet et al., 2012). In
and Magnoliaceae and the relationships among
this context, calibration is being recognized as a
Hernandiaceae, Lauraceae, and Monimiaceae are
critical point and can have a drastic influence on
still debated (Figure 1; Massoni et al., 2014). This
results (Inoue et al., 2010; Meredith et al., 2011;
group has a rich fossil record starting in the Early
Sauquet et al., 2012). Because of re-evaluation of
Cretaceous. Cretaceous fossils assigned to Mag-
the boundaries of geological time units, and some-
noliidae have been found in many parts of the
times re-dating of fossil beds, the accepted age of
world: South America (e.g., Mohr and Bernardes-
a fossil can change through time (Gandolfo et al.,
de-Oliveira, 2004; Mohr et al., 2013), North Amer-
2008). Therefore, an exhaustive geological review
ica (e.g., Dilcher and Crane, 1984; Crepet et al.,
is essential in order to provide an accurate mini-
2005), Europe (e.g., Friis et al., 2010, 2011), Asia
mum age (Parham et al., 2012). Except for recently
(e.g., Takahashi et al., 2001, 2008), Africa (e.g.,
developed total evidence dating approaches that
Doyle et al., 1990), Australasia (e.g., Dettmann et
combine the phylogenetic analysis of extant and
al., 2009), and Antarctica (e.g., Poole and Gott-
fossil taxa with the estimation of divergence times
wald, 2001; Eklund, 2003). Fossil Magnoliidae
(Pyron 2011; Ronquist et al., 2012), a review of the
come in a variety of forms, from wood (e.g., Heren-
phylogenetic position of a fossil is a second crucial
deen, 1991; Poole and Gottwald, 2001; Schöning
point in the calibration process (Gandolfo et al.,
and Bandel, 2004) and leaves (e.g., Upchurch and
2008; Parham et al., 2012; Sauquet et al., 2012).
Dilcher, 1990; Kvaček, 1992) to flowers (e.g., Dil-
Molecular scaffold approaches (analyzing morpho-
cher and Crane, 1984; Drinnan et al., 1990;
logical data with the topology of living taxa fixed by
Takahashi et al., 2008; Friis et al., 2011), fruits
a backbone constraint tree; Springer et al., 2001)
(e.g., Friis et al., 2010, 2011), seeds (e.g., Kno-
or total evidence approaches (using both molecular
bloch and Mai, 1986; Frumin and Friis, 1996), and
and morphological data; Kluge, 1989) can provide
pollen (e.g., Doyle et al., 1990; Macphail et al.,
a genuine test for the phylogenetic position of
1994). Because the number of characters
extinct taxa. A decision regarding the identity of the
observed in such fossils is often limited, establish-
node calibrated by a fossil has to take into account
ing their phylogenetic relationships to extant taxa is
the uncertainty of its phylogenetic position and the
not always straightforward. However, among fos-
uncertainty of the relationships among extant spe-
sils assigned to Magnoliidae, several are charac-
cies. A number of fossil taxa of Magnoliidae have
terized by good to exceptional preservation and a
already been included in morphological data matri-
large number of systematically useful characters,
ces and analyzed with a phylogenetic approach
such as the lignitized and charcoalified flowers
taking into account both morphological and molec-
considered here.
ular data (e.g., Doyle and Endress, 2010; von
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PALAEO-ELECTRONICA.ORG
TABLE 1. Summary of the calibration points provided in the present paper. Abbreviations: Ma, million anni.
Fossil Taxon Node Minimum Age
Endressinia brasiliana Crown-group Magnoliineae (Doyle and Endress, 2010; Mohr et al., 2013) 112.6 Ma
Schenkeriphyllum glanduliferum Crown-group Magnoliineae (Mohr et al., 2013) 112.6 Ma
Archaeanthus linnenbergeri Stem Magnoliaceae (Doyle and Endress, 2010) 96.5 Ma
Virginianthus calycanthoides Crown-group Laurales (Doyle et al., 2008) 107.7 Ma
Lovellea wintonensis Crown-group Laurales (Dettmann et al., 2009) 100.1 Ma
Jerseyanthus calycanthoides Crown-group Calycanthoideae (Crepet et al., 2005) 85.8 Ma
Cohongarootonia hispida Crown-group core Laurales (von Balthazar et al., 2011) 107.7 Ma
Mauldinia mirabilis Crown-group core Laurales (Doyle and Endress, 2010) 95.5 Ma
Walkeripollis gabonensis Crown-group Canellales (Doyle and Endress, 2010) 125.9 Ma
Saururus tuckerae Stem node of extant Saururus (Smith and Stockey, 2007) 44.3 Ma
Balthazar et al., 2011). These previous studies Heimhofer et al., 2005, 2007; Hochuli et al., 2006),
should, in principle, allow firm calibration of a which belonged to the same Southern Laurasian
molecular time scale, which is currently lacking for phytogeographic province of Brenner (1976; see
Magnoliidae (Forest and Chase, 2009). Doyle, 1969a, 1977, 1992; Wolfe and Pakiser,
The purpose of the present study is to provide 1971; Doyle and Hickey, 1976; Doyle and Robbins,
a reliable calibration scheme for the Magnoliidae, 1977; Christopher, 1979; Christopher et al., 1999;
usable as a starting point for any molecular dating Christopher and Prowell, 2010). Some of these
study of Magnoliidae or subgroups of this clade, as fossils, or others from the same localities, have
well as higher-level angiosperm divergence time been used for calibration in previous molecular dat-
studies. To do so, we have reviewed the geologic ing studies (Doyle et al., 2004; Magallón and Cas-
age and phylogenetic relationships of all fossils of tillo, 2009; Clarke et al., 2011; Pirie and Doyle,
Magnoliidae that have been included in at least 2012). In some cases, Clarke et al. (2011) pro-
one phylogenetic analysis (10 fossils, Table 1). For posed much younger minimum ages than those
this paper, we did not re-examine the fossil speci- recommended here because of conflicting conclu-
mens. Instead, our argumentation is based on pre- sions of earlier authors on the phylogenetic posi-
viously published descriptive and phylogenetic tion of fossils or on stratigraphic correlations. We
studies. Nine of these are represented by fossil argue that these minimum ages can be improved
flowers, in four cases with associated vegetative with critical examination. Our treatment includes a
parts, but one (Walkeripollis gabonensis) is based review of the age of units in the Atlantic Coastal
on dispersed pollen grains that have a particularly Plain, the source of four of the fossils treated here,
diagnostic combination of characters. Following a and several non-magnoliid taxa used in other dat-
strict minimum age philosophy, we propose to cali- ing analyses, which has been a subject of recent
brate the most recent common ancestor of all most discussion (Hochuli et al., 2006).
parsimonious assignments of previous analyses, Absolute ages used here follow Ogg and Hin-
and we provide associated synapomorphies when nov (2012). This chapter of the revised Geologic
they were mentioned in the original study. Time Scale of Gradstein (2012) is the most recent
Most of the fossils treated here are from conti- comprehensive synthesis of absolute dates for the
nental deposits that contain neither marine fossils Cretaceous, including estimated ages for each
that would allow direct correlation with the marine- substage, which we derive here from the charts in
based relative time scale, nor minerals suitable for figure 27.6 of Ogg and Hinnov (2012). When possi-
absolute radiometric dating. In most cases, their ble, use of substage boundaries is preferable to the
ages are based on indirect palynological correla- use of stage boundaries only, which can be overly
tions with pollen and spore sequences that are conservative when dealing with stages as long as
dated by marine fossils. For example, for the US the Albian (ca. 12.5 Ma). In their table 27.2, Ogg
Atlantic Coastal Plain, these reference sections are and Hinnov (2012) included the estimated uncer-
in the US Western Interior and Gulf Coast (Hed- tainty for the boundaries of stages (2-sigma), but
lund and Norris, 1968; Ward, 1986; Ludvigson et not for the boundaries of substages. In order to be
al., 2010) and western Europe (Góczán et al., conservative and to take into account existing esti-
1967; Kemp, 1970; Laing, 1975; Hughes, 1994; mates of uncertainty, those of our recommended
3
MASSONI, DOYLE, & SAUQUET: MAGNOLIIDAE
minimum ages that correspond to stage boundar- NODE 1: CROWN-GROUP MAGNOLIINEAE
ies are the point estimates of Ogg and Hinnov
Fossil Taxon 1 (preferred, given current
(2012) minus the associated two standard devia-
knowledge)
tions. Many radiometric dates are available for the
Late Cretaceous, thanks particularly to the abun- Endressinia brasiliana Mohr and Bernardes-de-
dance of bentonites. There are fewer radiometric Oliveira, 2004
dates for the Early Cretaceous, but there has been Node Calibrated. Crown-group Magnoliineae
much progress in integrating these with sequence (Doyle and Endress, 2010; Mohr et al., 2013)
stratigraphy, magnetostratigraphy, isotope stratig- Reference Specimen. MB. PB. 2001/1455 in
raphy, and cyclostratigraphy (which relates cyclic Museum of Natural History, Institute of Paleontol-
sedimentation to astronomical cycles of the earth’s ogy, Berlin, Germany (holotype; branching axis
orbit and tilt). Significantly younger ages and with attached leaves and flowers).
shorter durations for several stages were proposed Phylogenetic Justification. A molecular scaffold
by Fiet et al. ( 2006) based on K/Ar glauconite analysis by Doyle and Endress (2010), including
dates and cyclostratigraphy. Scott et al. (2009) 64 extant taxa sampled across angiosperms and
suggested that these ages may be too young due 142 morphological characters, placed Endressinia
to argon leakage, a problem in glauconites, and in seven different most parsimonious positions: all
Fiet et al. (2006) recognized that they require test- positions within the crown group of the clade
ing with studies on bentonites. By contrast, Huang Himantandraceae + Degeneriaceae + Eupomatia-
et al. (2010), also using cyclostratigraphy, obtained ceae + Annonaceae (each represented as one ter-
ages for the Aptian and Albian very close to those minal), or as the sister group of this clade. These
of Ogg and Hinnov (2012) and suggested that the relationships were supported by one unequivocal
shorter durations of Fiet et al. (2006) were due to synapomorphy, the presence of glands on the sta-
incompleteness of the sections studied. The dates mens or staminodes (Doyle and Endress, 2010). A
of Ogg and Hinnov (2012) still involve considerable more recent molecular scaffold analysis (Mohr et
extrapolation, but use of this single comprehensive al., 2013), which used a modified version of the
scheme should make correction of the calibrations morphological data set of Doyle and Endress
presented here easier if this becomes necessary in (2010) reduced to Magnoliales, Laurales, and
the future. Canellales (as outgroup), placed Endressinia as
We organized the present text by sections on the sister group of Schenkeriphyllum glanduliferum
calibrated nodes. When several fossil species were (another fossil from the same deposit, discussed
available to calibrate the same node, we used the below), with the clade of the two fossils being the
oldest (reported as the “preferred fossil” section in sister group of Magnoliaceae. Endressinia and
the text) to define the age associated with the cali- Schenkeriphyllum were united by sessile leaf blade
bration. The remaining extinct species that could (a new character) and linked with Magnoliaceae by
be used to calibrate the same node are reported as sheathing leaf base and dry fruit wall. As noted by
“additional fossils.” We organized the “additional Mohr et al. (2013), Doyle and Endress (2010) did
fossil” sections following the same structure used not score Endressinia as having a sheathing leaf
for the “preferred fossil” section. We proceeded in base. This was probably because the sheath was
this way because future phylogenetic and strati- formed from the unusual sessile leaf blade, rather
graphic studies may refine or modify the position or than a leaf base separated from the blade by a pet-
the age of the fossils, leading to future improve- iole, but this difference does not rule out homology
ment of the current scheme. This is especially rele- of the character. We have not attempted to resolve
vant when the older fossils are less completely this conflict with a new analysis. The implications
known than the younger ones. We also believe that for dating are complicated by the fact that the posi-
reporting the complete details of redundant fossils tion of Magnoliaceae within Magnoliales is still
identified as suitable calibrations is useful to debated. Two alternative positions have been sup-
increase confidence in the proposed calibration of ported by most analyses: either as the sister group
the corresponding nodes. of a clade of Degeneriaceae + Himantandraceae
(Soltis et al., 1999, 2007; Qiu et al., 2000, 2005,
2006; Savolainen et al., 2000; Zanis et al., 2002,
2003), or sister to a clade of Degeneriaceae +
Himantandraceae + Eupomatiaceae + Annona-
ceae (Doyle and Endress, 2000; Sauquet et al.,
4
PALAEO-ELECTRONICA.ORG
FIGURE 1. Simplified phylogenetic tree of Magnoliidae, after Massoni et al. (2014). Hydnoraceae (Piperales) are
excluded, because the family was not included in original publications positioning the 10 fossils considered here.
Colored boxes summarize the positions of fossils reviewed in the present paper. Their specific positions are figured
by small branches with the number of the corresponding fossil at the tip. These correspond to the most parsimonious
position(s) found for each fossil in previous phylogenetic analyses (see text for details). The minimum ages provided
by the fossils are presented at the nodes they calibrate. The dashed branch refers to the phylogenetic uncertainty
about relationships among Hernandiaceae, Lauraceae, and Monimiaceae (the position of Fossil 7 is on a branch not
represented here, corresponding to a different set of relationships among these three families). Fossils are num-
bered following their order in the text. Abbreviations: Ma, million anni.
5
MASSONI, DOYLE, & SAUQUET: MAGNOLIIDAE
2003). However, the results of both Doyle and Node Calibrated. Crown-group Magnoliineae
Endress (2010) and Mohr et al. (2013) support a (Mohr et al., 2013)
position of Endressinia within the crown group of Reference Specimen. MB. Pb. 1999/2356 in
Magnoliineae, the well-supported clade of five fam- Museum of Natural History, Institute of Paleontol-
ilies that is sister to Myristicaceae (Sauquet et al., ogy, Berlin, Germany (holotype; branching axis
2003), and each study alone leads to use of this with leaves and flowers).
fossil to calibrate the crown node of this clade. Additional Specimens. MB Pb. 2008/350. Para-
Therefore, Endressinia provides a safe minimum type (branching axis with leaves and flowers; will
age for the crown node of Magnoliineae (Figure 1). be deposited at the Geosciences Institute of the
Minimum Age. Aptian-Albian boundary, 112.6 Ma University of São Paulo, Brazil, and is being stored
(113 ±0.4 Ma) with the number GP/3T2442).
Age Justification. The fossil considered here was MB.Pb. 2002/1336 (specimen with poorly pre-
collected from the Crato Formation in the Araripe served flowers).
sedimentary basin of northeastern Brazil (Mohr et MB. Pb. 1997/1219 (twigs with attached leaves).
al., 2013). Mohr and Bernardes-de-Oliveira (2004) MB. Pb. 1999/575, 1999/577A plus 1999/577B
assumed that the Crato Formation is late Aptian or (dispersed leaves).
early Albian in age, based on numerous previous Phylogenetic Justification. As discussed for
estimates (e.g., Pons et al., 1996). Because of this Endressinia (Fossil 1), the molecular scaffold anal-
uncertainty, Clarke et al. (2011) proposed a mini- ysis of Mohr et al. (2013) placed Schenkeriphyllum
mum age for the Crato of 98.7 Ma, the top of the glanduliferum in a single most parsimonious posi-
Albian. However, evidence has been accumulating tion, together with Endressinia brasiliana, as sister
in favor of a late Aptian age (Coimbra et al., 2002). to the Magnoliaceae. This result implies that
Most recently, using gymnosperm pollen and dino- Schenkeriphyllum provides a minimum age for the
flagellates to correlate with better-dated sections, stem node of Magnoliaceae or the crown node of
Heimhofer and Hochuli (2010) concluded that the Magnoliineae, which are the same in the reference
Aptian-Albian boundary lies above the Crato For- backbone tree used by Mohr et al. (2013). Because
mation, and this was accepted by Mohr et al. the position of Magnoliaceae with respect to
(2013). We therefore propose a minimum age of Himantandraceae + Degeneriaceae and Eupomati-
112.6 Ma for Endressinia, the Aptian-Albian bound- aceae + Annonaceae remains unresolved, as dis-
ary (113 ±0.4 Ma; Ogg and Hinnov, 2012). cussed under Endressinia (Soltis et al., 1999,
Previous Use as Calibration. Endressinia has 2007; Doyle and Endress, 2000; Qiu et al., 2000,
been used in several molecular dating studies with 2005, 2006; Savolainen et al., 2000; Zanis et al.,
different ages and as a calibration for different 2002, 2003; Sauquet et al., 2003), and the position
nodes than recommended in the present study. In of Endressinia is debated (see phylogenetic justifi-
order to estimate divergence times within angio- cation for Endressinia; Doyle and Endress, 2010;
sperms, Magallón and Castillo (2009) used Mohr et al., 2013), we propose to use the age of
Endressinia with a similar age (112 Ma) but applied Schenkeriphyllum conservatively as a minimum
this age to the stem lineage of Magnoliineae. The age for crown group Magnoliineae (Figure 1).
same age was used by Pirie and Doyle (2012) to Minimum Age. Aptian-Albian boundary, 112.6 Ma
fix the age of the stem node of the clade of Eupo- (113 ±0.4 Ma)
matiaceae and Annonaceae, sister to Magnolia- Age Justification. Schenkeriphyllum was col-
ceae in their study. Surveswaran et al. (2010) used lected from the same sedimentary unit as Endres-
the fossil to provide a minimum age for the same sinia, the Crato Formation in the Araripe basin of
stem lineage corresponding, in their study, to the northeastern Brazil (Mohr et al., 2013). As dis-
same node recommended here (crown node Mag- cussed for Endressinia (Fossil 1), we propose a
noliineae). However, they used an age of 115 Ma. minimum age of 112.6 Ma, the Aptian-Albian
Finally, Couvreur et al. (2011) calibrated the same boundary (113 ±0.4 Ma; Ogg and Hinnov, 2012),
node (crown node Magnoliineae) with the same for this fossil, based especially on palynological
age but using it as a fixed age constraint. correlations by Heimhofer and Hochuli (2010).
Previous Use as Calibration. None to our knowl-
Fossil Taxon 2 (additional)
edge.
Schenkeriphyllum glanduliferum Mohr, Coiffard,
and Bernardes-de-Oliveira, 2013
6
PALAEO-ELECTRONICA.ORG
Fossil Taxon 3 (additional) fruit (shared with Magnolioideae). By contrast, a
recent cladistic analysis by Romanov and Dilcher
Archaeanthus linnenbergeri Dilcher and Crane,
(2013) positioned Archaeanthus sister to the Late
1984
Cretaceous seed genus Liriodendroidea (Frumin
Node Calibrated. Stem Magnoliaceae (Doyle and
and Friis, 1996) and identified the clade made up
Endress, 2010)
of these two extinct genera as the sister group of
Reference Specimen. UF 15703-4152 in Univer-
Liriodendron, supported by four synapomorphies.
sity of Florida, Gainesville, USA (holotype of
This would imply that Archaeanthus provides a
Archaeanthus linnenbergeri Dilcher and Crane;
minimum age for crown-group Magnoliaceae.
multifollicular fruit and proximal reproductive and
However, the taxonomic sampling of this analysis
vegetative portions of the same axis).
was very limited, as the extant taxa included only
Additional Specimens. UF 15703; 2300, 2317,
Magnoliaceae s.s. (= Magnolioideae) as a supra-
2318, 2590, 3022, 3837, 3907, 4105, 4112, 4134-
specific terminal, Liriodendron, and Illicium (Aus-
4150, 4152, 4153, 4155-4158, 4163, 4164, 4166-
trobaileyales), which is many nodes more distant
4170, 4198, 4532-4534: other specimens of
from Magnoliaceae than are other members of the
Archaeanthus linnenbergeri examined in Dilcher
order Magnoliales. In addition, one of the four pro-
and Crane (1984).
posed synapomorphies of Archaeanthus and Lirio-
UF 15703-3179 (holotype of Archaepetala beekeri
dendron, whorled perianth phyllotaxis, vs. spiral in
Dilcher and Crane; perianth parts).
Illicium and Magnolia, appears to be a symplesio-
UF 15703-3882. Other specimen of Archaepetala
morphy in Magnoliales, where the perianth is basi-
beekeri examined in Dilcher and Crane (1984).
cally whorled and trimerous (Endress and Doyle,
UF 15703-2266 (holotype of Archaepetala obscura
2009). Furthermore, although the perianth is spiral
Dilcher and Crane; perianth parts).
in some species of Magnolia s.l., in many species it
UF 15703-2747 (holotype of Kalymnanthus walkeri
is whorled (e.g., M. denudata: Erbar and Leins,
Dilcher and Crane; bud-scales).
1981). Two other proposed synapomorphies,
UF 15703-4114, UF 15703-4115. Other specimens
bilobed leaf apex and leaf lobation, are not inde-
of Kalymnanthus walkeri examined in Dilcher and
pendent characters, since the only lobation in the
Crane (1984).
leaf of Archaeanthus is that of the apex; its origin
UF 15703-2272 (holotype of Liriophyllum kansense
requires only one change, not two. The status of
Dilcher and Crane; leaves).
the fourth synapomorphy, fruitlets shed from the
UF 15703; 2267, 2271-2277, 2309, 2456, 2463-
receptacle, is uncertain, since Degeneria and most
2466, 2469-2471, 2473, 2475-2477, 2479, 2480,
Annonaceae also have this feature (van Setten
2482, 2484, 2485, 2487, 2488, 2492, 2493, 2679,
and Koek-Noorman, 1992). These observations
2948, 3443, 2813, 3816-3818, 3823, 3826, 3827,
imply that there are no more acceptable synapo-
3836, 3839, 3859, 3885, 3886, 3890, 3894, 3895,
morphies of Archaeanthus and Liriodendron in the
3992, 4028, 4029, 4051, 4120. Other specimens of
Romanov and Dilcher (2013) data set than in Doyle
Liriophyllum kansense examined in Dilcher and
and Endress (2010).
Crane (1984).
Even though we cannot dismiss the possibility
Phylogenetic Justification. The position of
that future analyses, based on denser taxon sam-
Archaeanthus linnenbergeri was investigated by
pling and better knowledge of the phylogenetic
Doyle and Endress (2010), in a molecular scaffold
position of Magnoliaceae, may eventually support
analysis in which the family Magnoliaceae (ca. 227
a position of Archaeanthus within crown-group
species) was split into two taxa: Magnolioideae,
Magnoliaceae, we prefer to be conservative and
often treated by recent authors as the single genus
recommend the use of Archaeanthus to serve as a
Magnolia, and Liriodendron. This analysis placed
minimum age constraint for the stem node of Mag-
Archaeanthus in three different most parsimonious
noliaceae. In the current consensus tree presented
positions: one as the sister group of Magnoliaceae
in Figure 1, this is the same node as crown-group
as a whole, and two within crown-group Magnolia-
Magnoliinae (the larger clade of five families found
ceae, either sister to Liriodendron or sister to Mag-
by Doyle and Endress, 2010; Sauquet et al., 2003).
nolioideae. The clade of Archaeanthus and
However, this is not the case in one of the resolved
Magnoliaceae was supported by three unambigu-
trees of Massoni et al. (2014) on which this con-
ous synapomorphies: sheathing leaf base, bilobed
sensus tree is based, in which Magnoliaceae are
stipules, and elongate receptacle, while the posi-
the sister group of the clade consisting of Degene-
tions within the family were supported by bilobed
ria (Degeneriaceae) and Galbulimima (Himantand-
leaf apex (shared with Liriodendron) or dehiscent
7
MASSONI, DOYLE, & SAUQUET: MAGNOLIIDAE
raceae). Furthermore, maintaining a distinction County, just to the east, the lower part of the third
between the two nodes may be useful because the cycle is represented by Dakota continental beds
association of Archaeanthus with Magnoliaceae that interfinger with marine rocks to the west.
appears to be more strongly supported than that of Because we cannot exclude the possibility that the
Endressinia (and Schenkeriphyllum) and less likely Linnenberger flora is from the lower part of the third
to change in future analyses. cycle, which Ludvigson et al. (2010) dated as early
Minimum Age. Early-middle Cenomanian bound- Cenomanian, we propose a conservative minimum
ary, 96.5 Ma age of 96.5 Ma for Archaeanthus, the early-middle
Age Justification. All the specimens used to Cenomanian boundary (no uncertainty provided;
describe Archaeanthus linnenbergeri come from Ogg and Hinnov 2012).
the Dakota Formation at the Linnenberger Ranch Previous Use as Calibration. Archaeanthus has
in Russell County, central Kansas, USA (Dilcher been used to provide calibration points within Mag-
and Crane, 1984). This formation lies between the noliidae in studies focused on angiosperms
underlying Kiowa Shale of Albian age and the over- (Magallón and Castillo, 2009) and on Annonaceae
lying Graneros Shale (Retallack and Dilcher, 2012) (Doyle et al., 2004; Richardson et al., 2004; Pirie et
of Cenomanian age. It has been traditionally al., 2006; Couvreur et al., 2008; Erkens et al.,
divided into two members, the Terra Cotta Clay 2009; Su and Saunders, 2009; Pirie and Doyle,
Member below and the Jansen Clay Member 2012). The great majority of these analyses used
above (Plummer and Romary, 1942). The beds this fossil as a minimum age constraint of 98 Ma for
containing the specimens considered here were the node recommended in the present study (stem
assigned to the Jansen Clay Member (Dilcher and Magnoliaceae; Doyle et al., 2004; Richardson et
Crane, 1984). Dilcher and Crane (1984) consid- al., 2004; Pirie et al., 2006; Couvreur et al., 2008;
ered the age of this locality to be latest Albian to Erkens et al., 2009; Su and Saunders, 2009). Only
earliest Cenomanian. However, D.L. Dilcher (pers. Magallón and Castillo (2009) used the age we rec-
comm. in Doyle and Endress, 2010) argued that it ommend (96.5 Ma), whereas Pirie and Doyle
is more likely latest Albian, based on a carbon iso- (2012) used an age of 100 Ma.
tope and sequence stratigraphic study by Gröcke
et al. (2006) at the Rose Creek locality in NODE 2: CROWN-GROUP LAURALES
Nebraska, where a flora described by Upchurch
Fossil Taxon 4 (preferred, given current
and Dilcher (1990) lies just below the Albian-Ceno-
knowledge)
manian boundary, plus the fact that the Dakota is
transgressive toward the east and sites such as Virginianthus calycanthoides Friis, Eklund, Peder-
Russell County are among its most western expo- sen and Crane, 1994
sures. A latest Albian age was accepted by Doyle Node Calibrated. Crown-group Laurales (Doyle et
and Endress (2010) and reaffirmed without discus- al., 2008)
sion by Romanov and Dilcher (2013). However, Reference Specimen. PP43703 in Field Museum
although the Rose Creek and Linnenberger Ranch of Natural History, Chicago (holotype; flower).
floras were both assigned to the Jansen Clay Phylogenetic Justification. Friis et al. (1994)
Member and considered roughly coeval by Farley assigned Virginianthus calycanthoides to the stem
and Dilcher (1986), their equivalence needs reex- lineage of Calycanthaceae because it resembles
amination in light of detailed sequence strati- extant Calycanthaceae (including Idiospermum)
graphic and palynological analyses of the Dakota but is more plesiomorphic in characters such as
Formation in Kansas, Nebraska, and Iowa by Lud- monosulcate rather than disulculate pollen. This
vigson et al. (2010). This study showed that the assignment was questioned by Crepet et al. (2005)
Dakota does not represent a simple transgressive based on a combined (total evidence) analysis of a
sequence but rather three transgressive-regressive data set of Renner (1999), which included 15 mor-
cycles. The first two cycles (equivalent to Palynos- phological characters, sequences of six molecular
tratigraphic Units 1 and 2) are late Albian, while the markers, 25 taxa of Laurales, and three outgroups.
third (Units 3 and 4) is early and middle Ceno- This analysis identified Virginianthus as the sister
manian; the boundary recognized by Gröcke et al. group of either Laurales as a whole or all Laurales
(2006), between the second and third cycles, falls other than Calycanthaceae. A molecular scaffold
within beds formerly assigned to the Jansen Clay analysis by Doyle et al. (2008), incorporating 65
Member. Unfortunately, this analysis did not extend morphological characters and using the same
as far west as Russell County, although in Lincoln backbone trees as Doyle and Endress (2010),
8
PALAEO-ELECTRONICA.ORG
found two alternative most parsimonious positions relations and incompletely controlled species
for this fossil, one sister to Calycanthaceae, the ranges, as argued by Hochuli et al. (2006).
other sister to the clade formed by all remaining Clarke et al. (2011) proposed a much younger
Laurales. The first position was supported by minimum age for Puddledock, 92.7 Ma, or the top
extended anther connective and the second by of the Cenomanian, based on the suggestion of
embedded pollen sacs. Positions sister to Laurales Hochuli et al. (2006) that Zone II extends into the
as a whole and nested within Calycanthaceae Cenomanian and the presence of late Cenomanian
were one step less parsimonious. Here we follow ammonites in the next younger unit, the Raritan
the result of Doyle et al. (2008) because it is based Formation of New Jersey (Cobban and Kennedy,
on a data set that included far more characters 1990). Hochuli et al. (2006) argued convincingly
than Crepet et al. (2005), many derived from in- that there is a significant break between Zones I
depth analyses of gynoecial morphology (e.g., and II in the Potomac sequence, since the early to
Igersheim and Endress, 1997). Both most parsimo- middle Albian interval in Portugal shows continuing
nious positions imply that Virginianthus provides a higher diversity of angiosperm monosulcates than
minimum age for the crown node of Laurales (Fig- tricolpates, whereas tricolpates are already more
ure 1). diverse at the base of Zone II. They argued that
Minimum Age. Middle-late Albian boundary, 107.7 Subzone II-B is late rather than middle Albian,
Ma based on the higher diversity of tricolpates than in
Age Justification. The fossil flower described by the Portuguese middle Albian and the presence
Friis et al. (1994) comes from the Potomac Group through Subzone II-B of the smooth tricolpate spe-
at the Puddledock locality in the Tarmac Lone Star cies Cupuliferoidaepollenites (Tricolpopollenites)
Industries sand and gravel pit 9 km southwest of parvulus, which they noted has not been reported
Hopewell, Prince George County, Virginia, USA. in dated sequences until the late Albian. However,
Friis et al. (1994, 1995) and von Balthazar et al. the reliability of C. parvulus is uncertain, since this
(2011) considered this locality early or middle species is rare in Subzone II-B and easy to over-
Albian, based on palynological correlation by R.A. look (for example, it was not reported by Brenner,
Christopher (in Dischinger, 1987) with the basal 1963). Furthermore, its first occurrences cited by
part of Potomac Subzone II-B of Brenner (1963) Hochuli et al. (2006) are in Canada, in the Northern
and Doyle and Robbins (1977) and the suggestion Laurasia province of Brenner (1976), where angio-
of Doyle (1992) that Subzone II-B may begin in the sperms were less abundant than in Southern Laur-
early Albian. However, an early Albian age for Sub- asia, and in deep sea cores. It is also possible that
zone II-B (and II-A) now appears unlikely in light of the higher diversity of angiosperms observed in the
palynological correlations by Hochuli et al. (2006) Potomac is partly a facies effect of comparing con-
with the well-dated marine Lower Cretaceous of tinental and marginal marine sequences. If angio-
Portugal and earlier work of Kemp (1970) on the sperms were locally dominant in some lowland
marine Albian of England (cf. Doyle et al., 2008). habitats but subordinate to ferns and gymno-
These studies support correlation of upper Zone I sperms at the regional scale (cf. Pierce, 1961;
with the basal early Albian of Portugal and the Doyle and Hickey, 1976), more angiosperms
early Albian of England, based on the appearance (including rare species) might be detected in a flu-
in all these intervals of reticulate tricolpate pollen vial sequence such as the Potomac Group than in
and Clavatipollenites rotundus (aff. Retimonocol- marine deposits like those in Portugal, where they
pites dividuus of Doyle and Robbins, 1977), as would be diluted by the higher regional production
argued by Doyle and Robbins (1977), but not stri- of fern spores and gymnosperm pollen. It is also
ate tricolpates, which appear later in the early likely that the contrast between diversity curves
Albian of Portugal (Hochuli et al., 2006). Consistent from the two sequences is exaggerated by the fact
with this, the Zone II index spore species Apicu- that the Portuguese curves were based on number
latisporis babsae of Brenner (1963) appears at the of species per sample, whereas the Potomac
base of the middle Albian in England (Kemp, curves were based on a range chart (Doyle and
1970). The conclusion of Doyle (1992) that the Robbins, 1977), so that species whose ranges
Zone I/II boundary lies well down in the Aptian was pass through the horizon of a given sample but
based largely on comparisons with Pennipollis were not found in that sample were treated as
(Brenneripollis) species and Schrankipollis in present.
Africa that appear to have involved too indirect cor- More positive evidence that much of Subzone
II-B is middle Albian comes from palynological cor-
9
MASSONI, DOYLE, & SAUQUET: MAGNOLIIDAE
relations with well-dated sequences in the US Gulf Fossil Taxon 5 (additional)
Coast and Western Interior, which were not consid-
Lovellea wintonensis Dettmann, Clifford, and
ered by Hochuli et al. (2006). Doyle (1977) showed
Peters, 2009
that the diverse angiosperm flora in the middle of
Node Calibrated. Crown-group Laurales (Dett-
Subzone II-B is especially similar at the species
mann et al., 2009)
level to that described by Hedlund and Norris
Reference Specimen. QMF51133 in the Palaeon-
(1968) in the “Walnut” Clay and Antlers Sand
tological Collection of the Queensland Museum,
(Fredericksburgian) of Oklahoma, which lies below
Queensland, Australia (Holotype, originally a com-
the middle-late Albian boundary defined by ammo-
plete specimen, now consisting of portions of a
nites in the overlying Goodland Limestone (Hed-
permineralized (silicified) flower/fruit in rock matrix
lund and Norris, 1968; Mancini and Puckett, 2005).
cut longitudinally into two slices and two thin sec-
Doyle and Robbins (1977) dated Subzone II-C as
tions: QMF51133 a-d).
latest Albian, but Hochuli et al. (2006) argued that it
Additional Specimens. QMF51134, QMF51135,
is Cenomanian, based on the psilate tricolporate
QMF51132. Other specimens used for the descrip-
species Tricolporoidites (Tricolporopollenites) dis-
tion (flowers/fruits).
tinctus and Tricolporoidites (Tricolporopollenites)
Phylogenetic Justification. A morphological par-
triangulus, which they stated first appear in the
simony analysis using the matrix of Doyle and
Cenomanian. However, most of the studies that
Endress (2000), with the exclusion of several taxa
Hochuli et al. (2006) cited considered only Ceno-
(eudicots, Piperales, Nymphaeales, monocots,
manian beds, not the latest Albian. More important,
Austrobaileya, Schisandraceae, and Illicium),
Ludvigson et al. (2010) listed psilate tricolporates
placed Lovellea wintonensis in one most parsimo-
(as Psilatricolporites sp.) in the latest Albian (Paly-
nious position sister to all Laurales excluding Caly-
nostratigraphic Unit 2) of the Dakota Formation
canthaceae (Dettmann et al., 2009). This “core
(see discussion of Archaeanthus, Fossil 3), and
Laurales” clade was well supported in previous
Laing (1975) recorded triangular grains similar to T.
studies (Soltis et al., 1999, 2000a, 2000b, 2007,
triangulus as Psilatricolpites rectilatibus in the
2011; Qiu et al., 1999, 2000, 2005, 2006, 2010;
marine upper Albian of France (Laing distinguished
Renner, 1999, 2004; Doyle and Endress, 2000;
P. rectilatibus from T. triangulus on lack of pores,
Savolainen et al., 2000; Zanis et al., 2002, 2003;
but the bent shape of the colpi in the Cenomanian
Nickrent et al., 2002; Hilu et al., 2003). Relation-
grain illustrated in his plate 90, figures 11-12 sug-
ships within the clade based on the morphological
gests that rudimentary pores were present).
analysis were not identical to those found in molec-
Together, these correlations lead us to consider
ular or combined morphological and molecular
that Virginianthus is of middle Albian age. There-
analyses (Doyle and Endress, 2000), but they are
fore, we use the middle-late Albian boundary,
consistent in supporting the monophyly of the Her-
107.7 Ma (no uncertainty provided; Ogg and Hin-
nandiaceae-Lauraceae-Monimiaceae clade
nov, 2012), as a minimum age for Virginianthus.
(though with the addition of Siparunaceae) and the
Previous Use as Calibration. Virginianthus has
position of Atherospermataceae and Gomortega-
been used in several large-scale studies (Magallón
ceae as outgroups to this clade (though as two
and Sanderson, 2005; Moore et al., 2007; Soltis et
successive branches rather than a clade). We con-
al., 2008; Bell et al., 2010). With the exception of
sider Lovellea wintonensis to provide a minimum
Magallón and Sanderson (2005), who used this
age for crown-group Laurales, or the stem node of
fossil to calibrate the crown node of Laurales with a
all Laurales except Calycanthaceae (Figure 1).
minimum age of 110 Ma, all these analyses used it
Minimum Age. Albian-Cenomanian boundary,
to calibrate the most recent common ancestor of
100.1 Ma (100.5 ±0.4 Ma)
Laurales and Magnoliales (i.e., the stem node of
Age Justification. Lovellea wintonensis comes
Laurales). Moore et al. (2007) used it to define a
from the basal part of the the Winton Formation, 48
minimum age of 113 Ma, Soltis et al. (2008) an age
km WNW of Winton, western Queensland, Austra-
fixed between 98 and 113 Ma, and Bell et al.
lia (Dettmann et al., 2009). Dettmann et al. (2009)
(2010) a minimum age of 98 Ma. In order to date
placed the sediments containing these fossils in
divergence times within Calycanthaceae, Zhou et
the Coptospora paradoxa or Phimopollenites pan-
al. (2006) used this species to calibrate the age of
nosus spore-pollen Zones of Helby et al. (1987)
the stem node of the family as at least 112 Ma.
based on the co-occurrence of Cicatricosisporites,
Crybelosporites, Clavatipollenites, and Phimopol-
lenites, indicating that they are no older than mid-
10