Canadian Journal of Earth Sciences
Phylogenetic relationships among the Rangeomorpha: The Importance of outgroup selection and implications for their diversification.
Journal: Canadian Journal of Earth Sciences
Manuscript ID cjes-2018-0022.R2
Manuscript Type: Article
Date Submitted by the Author: 01-Jul-2018
Complete List of Authors: Dececchi, Thomas; University of Pittsburgh Johnstown, Biology Greentree, Carolyn; Monash University, School of Earth, Atmosphere and EnvironmentDraft Laflamme, Marc; University of Toronto - Mississauga, Chemical and Physical Sciences Narbonne, Guy; Queen's University, Geological Sciences and Geological Engineering
Keyword: Ediacaran, Phylogenetics, Rangeomorpha, Evolution
Is the invited manuscript for consideration in a Special Not applicable (regular submission) Issue? :
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Phylogenetic relationships among the Rangeomorpha: The importance of outgroup
selection and implications for their diversification.
Dececchi, T.A. 1*, Narbonne G.M.2, Greentree, C.3, and Laflamme, M.4
1- Queen's University, Department of Geological Sciences and Geological
Engineering, Bruce Wing/Miller Hall, Kingston, ON, CAN
* Current affiliation: Biology Department, Natural Sciences Division,
University of Pittsburgh Johnstown, Johnstown, Pennsylvania, 15904, U.S.A.
[email protected] Draft
2- Queen's University, Department of Geological Sciences and Geological
Engineering, Bruce Wing/Miller Hall, Kingston, ON, CAN.
3- Monash University, School of Earth, Atmosphere and Environment, Clayton,
VIC, AUS. [email protected]
4- University of Toronto Mississauga, Department of Chemical & Physical Sciences,
Mississauga, ON, CAN. [email protected]
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1 Abstract
2 The Rangeomorpha are the oldest, most diverse, and most disparate clade of
3 Ediacaran macrofossils. Easily identifiable by their self-similar branching pattern,
4 they occupied epibenthic niche space ranging from the lowest tiered and recumbent
5 taxa up to meter-long upright fronds. A phylogenetic analysis using the largest and
6 most complete character set known for this group scored for 14 separate taxa was
7 undertaken to resolve their internal relationships and test previous hypotheses of
8 their evolutionary and ecological history. Owing to the lack of consensus on the
9 relationship amongst Ediacaran clades, several permutations with different
10 potential outgroup taxa were performed. Across these analyses, there is a strong
11 signal for an upright frondose ancestralDraft state for this clade, likely displaying
12 primary branches that were double sided, non-rotated, with the lower tiered and
13 recumbent forms being derived members of a single subclade. This has implications
14 on the life history reconstruction as well as taxonomic implications for this clade
15 and the origins of large multicellular life in the late Ediacaran.
16
17 KEYWORDS: Ediacaran, Phylogenetics, Rangeomorpha, Evolution
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24 Introduction
25 The Rangeomorpha represent the most diverse Ediacaran clade (Dececchi et al. 2017).
26 They are characterized by a modular and self-similar “fractal” branching pattern that
27 spans at least 4 orders of subdivisions, ranging from primary branches that are several
28 centimeters in size all the way down to fourth order, sub millimetre branching (Narbonne
29 2004; Liu et al. 2016; Kenchington and Wilby 2017). These modular elements are
30 combined into a diverse array of forms, from flat-lying mats to erect fronds, and range in
31 size from a few centimetres to well over a meter in length. Rangeomorpha occupied a
32 range of ecological niches (Clapham et al. 2003, Ghisalberti et al. 2014, Liu et al. 2015,)
33 time slices (Xiao and Laflamme 2008; Laflamme et al. 2013) and water depths (Boag et
34 al. 2016), suggesting they representedDraft a successful group prior to their demise in the
35 latest Ediacaran. They are particularly abundant and diverse in the post-Gaskiers
36 Conception and St. John’s groups in Newfoundland (Hofmann et al. 2008; Narbonne et
37 al. 2009; Liu and Matthews 2017), age-equivalent sections in Charnwood Forest in
38 England (Wilby et al. 2011), but are also found in northwestern Canada (Narbonne et al.
39 2014), and younger occurrences in the Flinders Ranges in South Australia (Gehling and
40 Droser 2013), Siberia (Grazhdankin et al. 2008), southern Namibia (Vickers-Rich et al.
41 2013), and central China (Chen et al 2014) . This ubiquity has led to the Rangeomorpha
42 being one of the most well studied members of the Ediacaran paleocommunity, with
43 research focusing on aspects of their architecture (Narbonne 2004; Narbonne et al. 2009:
44 Brasier and Antcliffe 2009; Brasier et al. 2012), growth (Gehling and Narbonne 2007;
45 Antcliffe and Brasier 2007, 2008; Flude and Narbonne 2008; Bamforth et al. 2008; Hoyal
46 Cuthill and Conway Morris 2014; Dunn et al. 2017), ecology (Clapham et al. 2003; Liu et
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47 al. 2015; Boag et al. 2016), population structure (Darroch et al. 2013) and even potential
48 reproductive mode (Mitchell et al. 2015). Despite these studies, evolutionary
49 relationships amongst the Rangeomorpha remain contentious (Brasier et al. 2012; Liu et
50 al. 2016; Dececchi et al. 2017).
51 Phlylogenetic approaches have previously been employed to explore the natural history
52 of the Rangeomorpha (Brasier and Antcliffe 2009; Dececchi et al. 2017). The present
53 paper expands on these studies to explore the effects that character definition, selection,
54 and variation have on Rangeomorpha alpha taxonomy, including testing previous
55 proposals for defining higher-order rankings (i.e. genus and above). Furthermore, a series
56 of standards for character construction and taxonomic classification within this clade is
57 proposed and applied to investigate Draftthe relationships among the Rangeomorpha.
58 Establishing a cladistic-based hypothesis for the internal relationships among
59 Rangeomorpha will help guide the understanding of the diversity of life prior to the
60 Cambrian explosion of complex metazoans (Erwin et al. 2011; Schiffbauer et al. 2016).
61
62 Methods
63 In order to create a well-supported phylogenetic hypothesis with a well-resolved
64 topology, it is recommended to incorporate characters derived from multiple axes of
65 information (development, growth, branch architecture, gross structural morphology,
66 etc.). In accordance with this proposal, and following the methodology of Dececchi et al.
67 (2017) in constructing a matrix of 19 distinct characters (Tables S1, S2) that fully
68 describe all morphological regions of known Rangeomorpha, and includes previously
69 proposed criteria for taxonomic differentiation (Brasier and Antcliffe 2009; Narbonne et
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70 al. 2009; Brasier et al. 2012).While this dataset is small compared to analysis of non-
71 Ediacaran taxa, it represents the most granular possible character resolution for these taxa
72 based on the available morphology. One major difference between this analysis and the
73 source data (Dececchi et al. 2017), beyond the addition of new taxa, is the modification
74 of several characters including changes in how growth polarity was previously defined by
75 Brasier et al. (2012) and expanding how growth is characterized and scored to reflect the
76 growth dynamics within the range of Rangeomorpha. The present paper uses the term
77 “polarity” as opposed to “terminal” from Dunn et al. (2017) due to the formers greater
78 prevalence in the literature, ease of use and the fact that the two do not differ in terms of
79 how one classifies the morphology of the taxa examined here. All characters were
80 unordered and unweighted in order toDraft reduce potential user bias. All phylogenetic
81 investigations were done in PAUP v. 4.0 (Swafford 2003) using the heuristic search
82 under default settings. Both the strict and majority rules consensus trees are presented to
83 illustrate both the most conservative topological reconstruction as well as one that are
84 found in the majority of trees, but due to the nature of the dataset with some taxa missing
85 data and the small number of OTU’s, may not be in 100% of reconstructions. This paper
86 uses parsimony over Bayesian approaches it may more accurately reflect how
87 morphological, as opposed to molecular data, functions (Goloboff et al. 2017, 2018).
88 All named taxa known from multiple specimens (5 or more) as well as several rare taxa
89 whose morphology may be informative for increasing topological resolution were
90 investigated and included in the analysis (Table S2). An expansive view of operational
91 taxonomic units (OTUs), including 14 named and 2 referred species as ingroup OTUs,
92 were included in the phylogenetic analysis in order to investigate recent proposals for
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93 synonymy/splitting in alpha taxonomy. The genus Fractofusus into F. misrai and F.
94 andersoni were differentiated based on the criteria identified by Gehling and Narbonne
95 (2007) as they show distinct branching architecture that may alter their phylogenetic
96 placement according to the architectural model. The single specimen
97 of Fractofusus from the Mackenzie Mountains (Narbonne et al. 2014) was scored as a
98 separate OTU in order to test its identification. Beothukis mistakensis and Culmofrons
99 plumosa were not synonymized and the so-called “MUN” frond (Liu et al. 2016) was
100 included as a separate OTU to test previous assertions of generic synonymy between
101 these three taxa (Liu et al. 2016; Dececchi et al. 2017).
102
103 To examine the effects of outgroup selectionDraft on internal relationships given the
104 uncertainty over the most likely sister taxon to the clade, the analyses was run using four
105 different outgroups: a member of the Arboreomorpha (Arborea arborea), two different
106 Erniettomorpha (Pteridinium simplex, Swartpuntia germsi), and two versions of an
107 artificial outgroup where the characters are set to the simplest state (as per Dececchi et al.
108 2017) that differed only in the presence of a surficial holdfast. This permits bracketing of
109 the possible effects of the still unknown sister group to Rangeomorpha, and also
110 examination whether differences in ancestral tiering strategy and method of attachment
111 altered the internal topology. Arborea and Swartpuntia are representatives of the upright
112 class of fronds (Narbonne et al., 1997; Laflamme et al., 2018), though not closely related
113 phylogenetically (Dececchi et al. 2017), with a well-developed holdfast and a petalodium
114 that would be placed in the water column while Pteridinium, though closer
115 phylogenetically to Swartpuntia represents distinct body form, a recumbent lower-tiered
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116 organism (Meyer et al. 2014; Darroch et al. 2015). To examine the level of support for
117 these relationships resampling was run without replacement or jackknifing (Siddell 2002)
118 for 10 and 20% of the character data to examine if a small number of characters were
119 having an extraordinary level of effect on the final topologies. The resulting figures, with
120 the exception of the Pteridinium permutation, strongly resemble the original trees (S1-5),
121 supporting the view that the tree topology is robust and that the character set is more than
122 adequate for the number of taxa analyzed.
123
124 Rangeomorphs have previously been subdivided into two major subgroups based on the
125 pattern of modular rangeomorph element arrangement along the stalk: the double-sided
126 rangid subgroup, in which each primaryDraft branch consists of secondary branches found
127 symmetrically on both sides of a central axis (strikingly similar to the “frondlets” of
128 Narbonne, 2004), and the single-sided charnids that consist of primary branches that are
129 asymmetrical (i.e. with secondary branches oriented downwards) (Narbonne et al. 2009;
130 Laflamme et al. 2012) or groupings based on branch rotation and furling (Brasier et al.
131 2012). It is our hope that these outgroups will help determine the robustness of the
132 proposed internal relationships among the Rangeomorpha, in addition to suggest a likely
133 plesiomorphic state with regards to water column subdivision and ecological tiering.
134
135 Results
136 Irrespective of outgroup chosen, there is consistently recover two distinct groupings
137 across the permutations: a group consisting of Charnia, Vinlandia, Trepassia and
138 Beothukis; and a group including Fractofusus, Bradgatia, Pectinifrons and the
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139 hapsidophyllid genera Hapsidophyllas and Frondophyllas. this unanimity reflects a
140 strong phylogenetic relationship among the taxa in these two clades. However, the
141 analyses also show that observed relationships between these two clades are critically
142 dependent on outgroup selection. The nature and significance of these findings are
143 discussed below.
144
145 Arborea as outgroup
146 A heuristic search of this taxonomic permutation resulted in 78 most parsimonious trees
147 (MPTs) of length 42 with a consistency index (CI) of 0.69 and a retention index (RI) of
148 0.764 (Fig. 1). A well-supported clade that corresponds to the traditional charnid group
149 (Narbonne et al. 2009 Charnia, Vinlandia,Draft Trepassia and Beothukis) with
150 Primocandelabrum as its most basal taxon. This group is characterized single sided
151 branching of the secondary branches and all taxa and furling of the first order branches in
152 taxa more derived than Primocandelabrum suggesting a shift in branching architecture
153 early on in this clade. The previously proposed rangid subgroup(Narbonne et al. 2009)
154 composed of double-sided primary branching fronds such as Rangea, Avalofractus,
155 Bradgatia and Fractofusus is not supported however, as Avalofractus is recovered as the
156 basalmost member of the Rangeomorpha with Rangea representing the basal form of the
157 rangids, though that relationship is only poorly supported and thus uncertain.
158 Hapsidophyllas, Pectinifrons, Bradgatia, Fractofusus, and Frondophyllas are united into
159 a universally-supported clade that houses a diverse combination of recumbent to tiered
160 forms. This group is likely unified in 1) the presence of more than one degree of growth
161 polarity (i.e. bi or multipolar per Brasier et al. 2012), 2) distal inflation of the second
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162 order branching, 3) the absence of a basal disc (though it is unknown in Frondophyllas),
163 4) double-sided secondary branches, and 5) lacking a stem (although traits 4+5 have a
164 wider distribution among the Rangeomorpha).
165
166 Pteridinium as outgroup
167 Using Pteridinium produces 103 MPT of a similar length (44 steps) and support indices
168 (CI=0.659, RI=0.732) to the Charniodiscus analysis. Under strict consensus there is little
169 resolution beyond the separation of the double-sided Hapsidophyllas, Pectinifrons,
170 Bradgatia and the Fractofusus species complex from the rest that remains in a polytomy.
171 Using majority rule consensus analysis, a more resolved topology with basal nodes
172 showing high, but not universal (99%)Draft support emerges (Fig. 2), the charnids are broken
173 up into a grade, not a single clade, with Charnia, Trepassia, Vinlandia at the base of
174 Rangeomorpha. A strongly-supported group was identified, with Beothukis at its base that
175 includes the traditional double-sided rangids as well as Culmofrons, MUN frond and
176 Primocandelabrum. Primocandelabrum appears to be their immediate outgroup to the
177 traditional rangids, whose basal members are Avalofractus and Rangea and a derived
178 grouping of primarily recumbent taxa. Beothukis is not united with the MUN frond and
179 Culmofrons in a single distinct clade, as these taxa are arranged as steps uniting the basal
180 charnids with the derived rangids.
181
182 Swartpuntia as outgroup
183 This permutations tree topology (Fig. 3) strongly resembles that of Arborea, differing
184 primarily in the placement of Rangea as the basal most rangeomorph, likely due to it
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185 having multiple petaloids similar to the outgroup. It displays a shorter tree (37 steps) for
186 28 MPT with similar support scores (CI of 0.676, RI of 0.739) than other permutations.
187
188 Artificial outgroup
189 Using the first artificial outgroup permutation (without a holdfast reconstructed),
190 produces 48MPT with a score of 40 (CI = 0.675, RI= 0.759). A separation of the upright
191 fronds (with the exception of Frondophyllas) from the recumbent or low tiered groups is
192 recovered, the latter of which is a polytomy under the strict consensus (Fig. 4). By
193 including the presence of a holdfast in the artificial outgroup (permutation 2) a strong
194 separation between the primarily upright fronds (charnids +Primocandelabrum + Rangea
195 + Avalofractus) and the recumbent/ Draftlower tiered double sided rangids (Fig, 5 a, b) is
196 shown. This gives similar tree scores to that using an artificial outgroup without a
197 holdfast (score 40, 139 MPT, CI = 0.675, RI= 0.759).
198
199 Discussion
200 A cladistic investigation into the internal subdivisions of the Rangeomorpha provides a
201 robust means of testing previous proposals more rooted in their gross phenotypes.
202 Interestingly, depending on the outgroup taxon used, one or both rangids and charnids are
203 either not recovered or recovered with some significant modifications. The selections of
204 outgroups permit evaluation of whether taxonomic or body plan differences play a
205 stronger influence on internal relationships within Rangeomorpha. When using a non-
206 upright frondose taxon, Pteridinium, produces a significantly different tree than do any of
207 the upright fronds. With Pteridinium the base of Rangeomorpha appears to comprise
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208 members of the charnids (Charnia-Trepassia-Vinlandia-Beothukis) which form a grade
209 into the traditional rangid (Fig. 2). This topology is likely driven by the fact that primary
210 morphology of the most basal members of charnids (Charnia-Trepassia-Vinlandia) have
211 constrained primary elements that are superficially convergent with the non-differentiated
212 primaries seen in the Erniettomorpha as well as having little to no recognized stem. This
213 convergence is not suspected to be homologous as Erniettomorphs and charnids are
214 constructed in significantly different ways (Laflamme and Narbonne 2008; Dececchi et
215 al. 2017) that are not captured by this analysis as it focuses on internal relationships
216 within the Rangeomorpha.
217
218 Outgroup selection appears to only Drafthave a minimal control on phylogenetic affinity and
219 final tree topology. Under the Arborea, Swartpuntia and both artificial outgroup
220 permutation, Avalofractus and Rangea are removed from association with other double-
221 sided forms (i.e. Fractofusus and Bradgatia) and placed either at the base of the chanrid
222 or the basal to the entire clade (Fig. 1,3-5). This challenges the recognition of the rangid
223 as a distinct group, especially as Avalofractus and Rangea are typically used as exemplar
224 taxa (Laflamme et al. 2012) and suggests instead that they represent a more
225 plesiomorphic state for the entire Rangeomorpha. Another possibility is that rangid is
226 restricted to those two taxa and all other double side taxa belong to a distinct clade that
227 has retained the ancestral double side morphology, though this would require redefining
228 the characteristics of rangid as presented in Laflamme et al. (2012). The strong similarity
229 between the topology of the Arborea and Swartpuntia and artificial permutations coupled
230 with Dececchi et al.’s (2017) finding that an upright frond is likely basal condition for
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231 Rangeomorpha, suggest than that the derived nature of the charnids seen in those
232 analyses is a more robust pattern then that seen using Pteridinium. Tellingly in no
233 analyses are the recumbent Fractofusus or Bradgatia reconstructed as basal members of
234 this clade contrary to previously suggestions that rangeomorphs were ancestrally lower
235 tiered, perhaps colonial, organism (Brasier and Antcliffe 2009). When coupled with the
236 finding that a holdfast (or similarly-enlarged basal structure) is found in members of
237 either potential sister clade Arboreomorpha (Jenkins and Gehling 1978) and the
238 Erniettomorpha (Darroch et al. 2015) it increases the likelihood that an upright, single
239 petalodium condition is ancestral for multiple groups of Ediacara biota.
240
241 The ancestral condition for RangeomorphaDraft is most parsimoniously reconstructed as an
242 upright frond with an exposed, double-sided (or unfurled per Brasier et al. 2012)
243 morphology to its branches. The presence Rangea and/or Avalofractus at the base of
244 either the entire clade or the base of the charnids in all but the Pteridinium permutation
245 implies that furled branches represent a derived feature within rangeomorphs. Although
246 this conclusion is not unanimous across all permutations, it is supported by the type
247 specimen of Trepassia (ROM 38628) that shows that new branches inserted at the apex
248 were originally double sided and poorly constrained, but that they rotated and became
249 more constrained in more mature branches towards the base of the frond (Narbonne et al.
250 2009). This pattern of growth potentially recapitulates the proposed evolutionary
251 continuum of branch rotation and constraint across the charnids subgrouping (Laflamme
252 et al. 2012). The recovery of the multibranched “network of leaves” taxa Hapsidophyllas
253 and Frondophyllas, which display a constrained branching pattern that resembles the one
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254 seen in Charnia (Bamforth and Narbonne 2009), nested well within a grouping of
255 double-sided branching argues for convergence in the evolution of single-sided branching
256 amongst the Rangeomorpha. This raises questions about the precise nature of the branch
257 rotation between these two groups.
258
259 The suggestion that the single-sided, constrained branching condition is a derived trait,
260 with a transitional series that includes Culmofrons through Beothukis and Trepassia,
261 agrees with previous workers (Narbonne et al. 2009; Laflamme et al. 2012). This
262 hypothesis does seem at odds with the first occurrence record, as the earliest known
263 Rangeomorpha are single-sided charnids, followed by the appearance of multiple double-
264 sided taxa 5 million years later (Liu Draftet al. 2012). However, the proposed reconstruction of
265 double-sided branching as ancestral for Rangeomorpha requires only a short ghost
266 lineage, far less than that observed among well-sampled vertebrate groups for example
267 (Clavin and Forey 2007; Benton et al. 2014; Brusatte and Carr 2016; Philips 2016). The
268 transition from an ancestral double-sided branching pattern towards a single-sided
269 branching architecture could be explained in many ways. The first is as a simplification
270 with the loss of the mirroring present in the ancestral double-sided element. Another
271 would be the evolution of a structureless primary branch from which rangeomorph
272 secondary branches sprout. If correct these two alternatives imply different evolutionary
273 trajectories. The first is simplification, a trend that is seen in other aspects of the anatomy
274 of these organisms such as the loss of holdfasts and stems in many derived rangids. The
275 other is the origin of a de novo branching style within the charnid subgrouping. Either
276 approach has implications for the growth, feeding, and tiering of the Rangeomorpha, and
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277 have implications for the ecological reconstructions as perhaps not all members of the
278 Rangeomorpha have the identical life histories.
279
280 Recent work has suggested that Ediacaran holdfasts are more complicated than
281 previously thought, possibly allowing for chemosymbiosis (Burzynski et al. 2017). Along
282 these lines, Dufour and McIllroy (2016) suggested that Fractofusus may have been at
283 least partially chemosynthetic. If correct this finding may have profound implications for
284 the clade as a whole since there is no major difference in morphology of the rangeomorph
285 branching pattern between Fractofusus and other Rangeomorpha with double-sided
286 primary branches including the basal members recovered here (Rangea and
287 Avalofractus). Nutrient acquisition Drafthas been suggested to have a role in the phenotypic
288 diversity of rangeomorphs (Laflamme and Narbonne 2008; Ghisalberti et al. 2014; Hoyal
289 Cuthill and Conway Morris 2017). Perhaps the high surface area to volume ratio of the
290 petalodium allowed for multiple feeding strategies ancestrally, which would have been
291 specialized in the derived recumbent taxa. Further work on this potential will impact
292 these reconstructions of the ecological complexity as different nutrient acquisition
293 methods may have been employed both inter- and potentially intraspecifically depending
294 on resource limitations.
295
296 These results also suggest that having more than one axis of enlargement (i.e. growth
297 axis) is derived from the ancestral unipolar state. Unipolar growth (i.e. growth along a
298 single plane) appears to be a common growth strategy for several Ediacaran groups
299 including Arboreomorpha (Laflamme et al. 2004), Erniettomorpha (Ivantsov et al. 2016;
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300 Dunn et al. 2017), Dickinsoniomorphs (Gold et al. 2015; Evans et al. 2017; Hoekzema et
301 al. 2017; Reid et al. 2017) and Bilaterialomorpha (Lin et al. 2006). However, given the
302 uncertainty in the evolutionary relationships between these groups (Erwin et al. 2011;
303 Dececchi et al. 2017), one cannot determine if this represents evolutionary convergence
304 or a deep homology across disparate clades. Furthermore, it should be noted that the
305 majority of rangeomorph taxa appear to have grown by branch/element inflation with
306 fewer examples of branch insertion/addition (Gehling and Narbonne 2007; Antcliffe and
307 Brasier 2007, 2008; Laflamme et al. 2007, 2012; Dunn et al. 2017). Thus, the term
308 polarity as used here reflects the direction of enlargement, either by inflation or insertion,
309 rather than necessarily the direction of new growth by segmental addition.
310 Draft
311 One interesting result is the implied pattern of early diversification soon after the rise of
312 the Rangeomorpha following the termination of the Gaskiers glaciation (Narbonne and
313 Gehling 2003; Liu et al. 2012; Narbonne et al. 2014), with some of the earliest known
314 specimens representing derived members of both branching strategies. It is of note that
315 younger Ediacaran assemblages (i.e. White Sea and Nama – Waggoner 2003; Boag et al.
316 2016) are characterized by a distinct loss in Rangeomorpha diversity and abundance,
317 especially in terms of lower-tiered and recumbent forms. This suggests a very rapid
318 radiation of Rangeomorpha bodyplans into an open (or minimally constrained) ecosystem
319 for macroscopic multicellular organisms (Narbonne et al. 2009; Cuthill Hoyal and
320 Conway Morris 2014). The loss of recumbent Rangeomorpha taxa could be explained by
321 several factors including competition with mobile metazoans found in the White Sea
322 (Paterson et al. 2017; Darroch et al. 2017) and Nama biotas (Darroch et al. 2015, 2016),
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323 bathometric factors as rangeomorphs migrated into shallow water settings (Grazhdankin
324 2004; Boag et al. 2016), are facies dependent (Wilby et al. 2015) or that the radiation of
325 recumbent Rangeomorpha represents a localized phenomenon with only a minor presence
326 beyond Avalonia.
327
328 Variation and taxonomy in Rangeomorpha
329 The extent to which interspecific variability should be accounted for both in character
330 state delineation and OTU selection is a source of concern in attempting to construct
331 characters for lineages of organisms whose affinities, physiologies, and developmental
332 biology are controversial. Two major sources of variation, ontogenetic and phenotypic,
333 have been suggested to be present inDraft these organisms (Liu et al. 2015; Kenchington and
334 Wilby 2017) and could influence multiple aspects of alpha taxonomy and ultimately
335 phylogeny. Building upon the work of Liu et al. (2016), the present paper proposes a
336 series of guidelines for the identification of these issues among the Ediacara biota, and
337 propose a series of best practices for how to account for them in future systematic and
338 phylogenetic studies.
339
340 The character set focuses strongly on features that do not appear to vary significantly
341 within complete specimens of a taxon across its known size classes or module counts,
342 taken here as signals for semiphorant categorisation amongst inflationary or insertion-
343 based growth taxa respectively. The exception to this guideline is the presence of a
344 holdfast (character 13), which, while variable between specimens, is thought to be driven
345 by preservation style rather than individual variation (Burzynski and Narbonne 2015,
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346 Burzynski et al. 2017). In this case if a single specimen for a given taxon was associated
347 with a holdfast it was scored as present for that taxon. The smallest known upright fronds
348 (Liu et al. 2012) and recumbent taxa (Gehling and Narbonne 2007; Flude et al. 2008;
349 Bamforth and Narbonne 2008) all show similar gross morphological features across size
350 ranges of a single taxon. One potential exception to this is Trepassia that shows variation
351 in branching pattern at their apex, showing double-sided morphology while the lower
352 (presumed) mature branches display a single-sided pattern (Narbonne et al. 2009). With
353 this possible exception, the characters used in this analysis do not show clear signs of
354 ontogenetic variation that could significantly influence the scoring or the topology of the
355 resulting trees.
356 Draft
357 Since ontogeny can lead to specimens with characters seen in more basal members of the
358 clade and lacking several derived features that would signal its true phylogenetic position,
359 it is important that different age classes of a single taxon not lead to different taxa once
360 investigated cladistically (Campione et al. 2012; Lamsdell and Selden 2013). This has led
361 some to suggest that paleontologists take a conservative approach to alpha taxonomy
362 (Benton 2008), however this can lead to overly broad attempts at synonymization
363 (“lumping”) and reduced phylogenetic resolution, especially in organisms with broad
364 geographic or stratigraphic ranges. In an attempt to minimize the potential for ontogeny
365 to overrun phylogeny, Longrich and Field (2012) put forth three testable criteria that need
366 to be met before suggesting synonymy based on ontogeny: 1) geographic/stratigraphic
367 overlap, 2) one taxon must be represented by more mature individuals than the other and
368 3) intermediates linking the two end members.
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369
370 There is little evidence that more than one purported species are simply members of an
371 ontogenetic continuum. One potential candidate for synonymization is Trepassia, but the
372 variation in frond architecture in the most distal primary branches of Trepassia
373 (Narbonne et al. 2009) is not supportive of this view. Trepassia grew by primary branch
374 insertion, which appears to be distinct from all other double-sided Rangeomorpha taxa
375 currently studied that instead display an inflationary mode of growth. Differences in
376 growth strategies appear early in development and are identifiable at even small size
377 classes and branch/module counts with size having very little to no relationship to branch
378 count (Gehling et al. 2000; Narbonne et al. 2009; Liu et al. 2012). This is because in
379 insertionary taxa branch number is aDraft factor in their indeterminate growth (Wilby et a.
380 2015; Dunn et al. 2017) while in inflationary taxa there is a cessation of addition of new
381 branches well before the largest size classes, indicating that while growth through
382 differentiation has ceased, growth through inflation has not. This early presence and
383 ubiquity across all size classes and localities for all taxa so far sampled suggest that this
384 trait is also independent of ontogeny, thus there is no evidence of switching between
385 growth styles with maturation. Therefore, currently there is little evidence that
386 ontogenetic variation has a significant influence on Rangeomorpha alpha taxonomy.
387
388 Another potential source of disparity is phenotypic plasticity leading to ecophenotypic
389 variation, where environmental differences cause non-heritable phenotypic divergence
390 between members of a single species (Whelan et al. 2012). This has been suggested to
391 occur in at least one lineage of Rangeomorpha (Liu et al. 2016) and may be applicable to
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392 many more of the currently recognized taxa (Hoyal Cuthill and Conway Morris 2017).
393 Thankfully there are several criteria that can be applied to Ediacaran systematic
394 descriptions before proposing synonymy of taxa through the invocation of ecophenotypic
395 variation. First off, specimens must be subjected to different environmental conditions.
396 Additionally, increased morphological discrepancy with ontogeny (Johnson 1981),
397 differentiation based on a single (or a select few) potentially correlated characters,
398 occurrence of intermediates across environmental gradients, and similar trends in other
399 closely related taxa should also ideally be demonstrated.
400
401 Following these criteria and the results of the cladistics analyses, the proposed synonymy
402 of Beothukis and Culmofrons (Liu etDraft al. 2016) is not supported. Importantly, both taxa are
403 found in close proximity on the same surfaces along the Mistaken Point Ecological
404 Reserve at Bristy Cove and Gull Rock Cove (Laflamme et al. 2012, Mason and Narbonne
405 2016). Furthermore, there is no evidence of increasing divergence between conditions
406 with increasing size, with features such as stem length showing increased differentiation
407 at smaller size classes. Using the data in Narbonne et al. (2009) and Laflamme et al.
408 (2012), stem length scales significantly differently (F=55.913, p(same)<0.0001). There is
409 no evidence for increased disparity with maturation as relative value differences is higher
410 at smaller size classes, with stems closer to 40% or more of total length, and invariably
411 remains above 29% of total length in Culmofrons while it remains below 5% in Beothukis
412 regardless of size class (Fig. 6). Additionally, the listed characters that distinguish
413 between Beothukis and Culmofrons, including significant disparity in stem length
414 proportions, the presence of a surficial holdfast (Burzynski and Narbonne 2015), and
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415 differences in the number of first order branches (and their arrangement) along the central
416 axis (Laflamme et al. 2012) are not suspected to be correlated (contra ecophenotypic
417 variation). The number of first order branches has been proposed to be an ontogenetic
418 feature (Liu et al. 2016) but as Beothukis and Culmofrons appear to grow by primary
419 branch inflation (not insertion; Narbonne et al. 2009; Laflamme et al. 2012), the number
420 of first order branches cannot represent an ontogenetically variable trait. Applying
421 previously recognized criteria across localities and taxa shows that the alpha diversity of
422 Rangeomorpha used here is not a by-product of phenotypic plasticity (contra Hoyal
423 Cuthill and Conway Morris 2017) and reflects real taxonomic differences.
424
425 Conclusions Draft
426 Rangeomorpha are among the most morphologically disparate and biologically diverse
427 Ediacaran clades. By characterizing and revising all known members of this clade with
428 more than 5 preserved specimens, it is possible to establish a robust dataset to study the
429 topology of the rangeomorph phylogenetic tree. Support is found for some existing
430 classification schemes (e.g. Narbonne et al. 2009; Brasier et al. 2012; Kenchington and
431 Wilby 2017), however, this study also demonstrates the need for caution when
432 interpreting evolutionary trends due to repeated convergences among divergent branches.
433 It is proposed that the ancestral condition for the Rangeomorpha was a double-sided
434 branched, unipolar frond, implying that the recumbent and multipolar Rangeomorpha are
435 derived members whose life habit may have differed significantly from basal frondose
436 forms. This study provides the framework for future analyses on evolutionary rates of
437 change as well as other biological traits that require a robust phylogeny. Both outgroup
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438 bodyplan and phylogenetic affinity in the outgroup taxa influence the arrangement of
439 internal nodal relationships of rangeomorphs, though the former may be a stronger factor
440 based on the current level of knowledge. Finally, this work helps establish the foundation
441 for methods in character construction to produce accurate and well-resolved trees. The
442 methods and best practice guidelines presented here should form the template for future
443 extensions of cladistic analysis of other Ediacaran groups.
444
445 Acknowledgements
446 We are grateful for funding through a William White Fellowship to T.A.D., NSERC
447 Discovery Grants to G.M.N. and M.L., and a Queen’ s Research Chair to G.M.N. We
448 also thank G. Burzynski for his helpfulDraft discussions.
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Figure captions
Figure 1: Phylogeny of Rangeomorpha using Arborea as the outgroup to polarize the
data. A) Strict consensus tree. B) Majority rule consensus tree. Numbers above nodes
represent percentage of trees supporting that node.
Figure 2: Phylogeny of Rangeomorpha using Pteridinium as the outgroup to polarize the
data. A) Strict consensus tree. B) MajorityDraft rule consensus tree. Numbers above nodes
represent percentage of trees supporting that node.
Figure 3: Phylogeny of Rangeomorpha using Swartpuntia as the outgroup to polarize the
data. A) Strict consensus tree. B) Majority rule consensus tree. Numbers above nodes
represent percentage of trees supporting that node.
Figure 4: Phylogeny of Rangeomorpha using an artificial outgroup, see text for details on
its composition. A) Strict consensus tree. B) Majority rule consensus tree. Numbers
above nodes represent percentage of trees supporting that node.
Figure 5: Phylogeny of Rangeomorpha using an artificial outgroup, though with the
presence of a holdfast included, though this is a derivate state in the matrix. A) Strict
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consensus tree. B) Majority rule consensus tree. Numbers above nodes represent percentage of trees supporting that node.
Figure 6: Regression of stem length versus total frond length, both in mm, based published specimens of both Culmofrons (closed circles) and Beothukis (open circles) from Narbonne et al. (2009) and Laflamme et al. (2012). Note the large number of specimens of Beothukis that show no stem development, recorded here as stem length of zero, across even the lowest size classes. This differs markedly from the condition in
Culmofrons where the smallest individuals tended to have proportionately longer stems, with stem length showing a slight negative allometric pattern.
Draft
Supplementary figure captions
S1: Jackknifed phylogeny of Rangeomorpha using Arborea as the outgroup to polarize
the data. A) 10% of characters dropped. B) 20% of characters dropped.
S2: Jackknifed phylogeny of Rangeomorpha using Pteridinium as the outgroup to polarize the data. A) 10% of characters dropped. B) 20% of characters dropped.
S3: Jackknifed phylogeny of Rangeomorpha using Swartpuntia as the outgroup to polarize the data. A) 10% of characters dropped. B) 20% of characters dropped.
S4: Jackknifed phylogeny of Rangeomorpha using an artificial outgroup to polarize the
data. A) 10% of characters dropped. B) 20% of characters dropped.
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S5: Jackknifed phylogeny of Rangeomorpha using using an artificial outgroup, though
with the presence of a holdfast included, to polarize the data. A) 10% of characters
dropped. B) 20% of characters dropped.
Draft
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Strict consensus tree Charnia
Vinlandia
Trepassia
Beothukis
MUN frond
Avalofractus
Culmofrons Draft Pectinifrons
Frondophyllas
Hapsidophyllas
Fractofusus andersoni
Fractofusus misrai
Fractofusus sp.
Bradgatia
Rangea
Primocandelabrum
Arborea
https://mc06.manuscriptcentral.com/cjes-pubs Page 35 of 48 Canadian Journal of Earth Sciences
Majority-rule consensus tree Charnia 100
100 Vinlandia
100 Trepassia
100 Beothukis
87 MUN frond
94 Culmofrons
Primocandelabrum Draft Avalofractus
Pectinifrons
74 Frondophyllas 100 77 Hapsidophyllas
Bradgatia 100
Fractofusus andersoni
54 68 Fractofusus misrai
Fractofusus sp.
Rangea
Arborea
https://mc06.manuscriptcentral.com/cjes-pubs Canadian Journal of Earth Sciences Page 36 of 48
Strict consensus tree Charnia
Trepassia
Vinlandia
Beothukis
Avalofractus
Culmofrons
Pectinifrons
Draft Frondophyllas
Hapsidophyllas
Fractofusus andersoni
Fractofusus misrai
Fractofusus sp.
Bradgatia
Rangea
MUN frond
Primocandelabrum
Pteridinium https://mc06.manuscriptcentral.com/cjes-pubs Page 37 of 48 Canadian Journal of Earth Sciences
Majority-rule consensus tree Charnia
Trepassia
Vinlandia
Beothukis
Avalofractus 66 Pectinifrons
77 Frondophyllas 100 83 84 Draft Hapsidophyllas
99 Bradgatia 100
Fractofusus andersoni
70 52 55 Fractofusus misrai
Fractofusus sp.
99 Rangea
Primocandelabrum 99
Culmofrons
MUN frond
Pteridinium https://mc06.manuscriptcentral.com/cjes-pubs Canadian Journal of Earth Sciences Page 38 of 48
Strict consensus tree Charnia
Vinlandia
Trepassia
Beothukis
MUN frond
Avalofractus
Culmofrons
Draft Pectinifrons
Frondophyllas
Hapsidophyllas
Fractofusus andersoni
Fractofusus misrai
Fractofusus sp.
Bradgatia
Rangea
Primocandelabrum
Swartpuntia https://mc06.manuscriptcentral.com/cjes-pubs Page 39 of 48 Canadian Journal of Earth Sciences
Majority-rule consensus tree Charnia 100
100 Vinlandia
100 Trepassia
100 Beothukis
70 MUN frond
85 Culmofrons
55 Primocandelabrum
Draft Avalofractus
Pectinifrons
91 76 Frondophyllas 100 82 Hapsidophyllas
Bradgatia 100
Fractofusus andersoni
55 Fractofusus misrai
Fractofusus sp.
Rangea
Swartpuntia https://mc06.manuscriptcentral.com/cjes-pubs Canadian Journal of Earth Sciences Page 40 of 48
Strict consensus tree Charnia
Vinlandia
Trepassia
Beothukis
MUN frond
Avalofractus
Culmofrons
Draft Rangea
Primocandelabrum
Pectinifrons
Frondophyllas
Hapsidophyllas
Fractofusus andersoni
Fractofusus misrai
Fractofusus sp.
Bradgatia
artificial outgroup https://mc06.manuscriptcentral.com/cjes-pubs Page 41 of 48 Canadian Journal of Earth Sciences
Majority-rule consensus tree Charnia 100
100 Vinlandia
100 Trepassia
100 Beothukis
71 MUN frond
85 Culmofrons
56 Primocandelabrum
100 Draft Avalofractus
Rangea
Pectinifrons
67 Frondophyllas 100 88 Hapsidophyllas
Bradgatia 62
Fractofusus andersoni
75 Fractofusus misrai
Fractofusus sp.
artificial outgroup https://mc06.manuscriptcentral.com/cjes-pubs Canadian Journal of Earth Sciences Page 42 of 48
Strict consensus tree Charnia
Vinlandia
Trepassia
Beothukis
MUN frond
Avalofractus
Culmofrons
Draft Pectinifrons
Frondophyllas
Hapsidophyllas
Fractofusus andersoni
Fractofusus misrai
Fractofusus sp.
Bradgatia
Rangea
Primocandelabrum
artificial outgroup with holdfast https://mc06.manuscriptcentral.com/cjes-pubs Page 43 of 48 Canadian Journal of Earth Sciences
Majority-rule consensus tree Charnia 100
100 Vinlandia
100 Trepassia
100 Beothukis
57 MUN frond
71 Culmofrons
Primocandelabrum
Draft Avalofractus
Pectinifrons
83 Frondophyllas 100 87 Hapsidophyllas
Bradgatia 100
Fractofusus andersoni
52 Fractofusus misrai
Fractofusus sp.
Rangea
artificial outgroup with holdfast https://mc06.manuscriptcentral.com/cjes-pubs Canadian Journal of Earth Sciences Page 44 of 48
Culmofrons y=0.25719x+0.84672
Draft
Beothukis y=0.067905x-1.6779
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Table 1 character list
1. Polarity (the number of apical growth tips within a single frondose organism): 0 unipolar 1 bipolar 2 multipolar
2. Petalodium number 0 single petalodium 1 multiple petalodia, each with a separate stalk or other division
3. Petaloid number (definition from Laflamme and Narbonne 2008) 0 2 petaloids, typically but not invariably creating a flat, single plane 1 multiple petaloids that are symmetrically arranged
4. inflation of first order 0 proximal 1 medial 2 moderate 3 distal Draft
5. Inflation of second order 0 proximal 1 medial 2 moderate 3 distal
6. Primary branches display branching pattern of "secondaries" rows (see Figure 3 in Laflamme et al. 2012), this arrangement shows: 0 no fractal divisions 1 rows displaying double-sided morphology 2 row displaying single sided morphology
7. Secondary branches display branching pattern of "tertiaries" rows (see Figure 3 in Laflamme et al. 2012), this arrangement is 0 secondaries not present or show no subdivisions 1 secondaries are double sided 2 secondaries are single sided
8. furled structure 1st order 0 no 1 yes
https://mc06.manuscriptcentral.com/cjes-pubs Canadian Journal of Earth Sciences Page 46 of 48
9. furled structure 2nd order 0 no 1 yes
10. growth axis 0 concealed 1 exposed
11. Subparallel (P) or radiate (R) or Irregular (I) 1st order 0 Subparallel 1 radiating 2 irregular
12. Subparallel (P) or radiate (R) or Irregular (I) 2nd order 0 Subparallel 1 radiating 2 irregular
13. presence of basal disc 0 absent Draft 1 present
14. Holdfast position (See Burzynski and Narbonne 2015 in relation to the sediment water interface and a larger discussion on differentiation this feature) 0 subsurface 1 surficial
15. Stem 0 absent/ minor, <5% total frond length 1 present >5% but less than 20% 2 >20%
16. Branches (primaries) constrained distally 0 absent 1 moderate 2 highly constrained-primaries bound to each other along length 3 distal tip of primary bound to marginal tubes or ridge
17. Branches (secondaries) constrained (box shape) 0 absent 1 present
https://mc06.manuscriptcentral.com/cjes-pubs Page 47 of 48 Canadian Journal of Earth Sciences
18. Presence of subsidiary frondlets (as per Gehling and Narbonne 2007) 0 absent 1 present
19. Growth pattern of new primaries 0 insertion 1 inflation 2 insertion then inflation
Draft
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19
18
17
2 - 0 1
15 15 16
14
1 0 1 0 0 1 0 0 1 0 0 1 0 1 0 0 0 0 ? 0 1 0 - 0 - 0 0 0 0 0 0 0 1 1 1 1 1 2 0 0 0 ?
0/1 0/1 0 1 1 2 0 0 0 1 0 0/1 1 0 1 0 0 0 1
11 11 12 13
0 0 0 0 0/1 0/1
? ? 1 1 1 0 1 0/1 0 1 ? 0/1 0 0 0 ? 0 ? - 0 ? 0 0 0 - 0 0 ? 0 0 0 0 1 0 0 - 0 2 1 ? 0 0 ? ? ? ? ?
8 1 9 1 1 10 1 1 0 1 1 0 0 0 1 0 0 0 1 0 0/1 0 0/1 1 0/1 0 0/1 1 0 0/1 0 0 0 0/1 0/1 0 0/1 2 1 1 0/1 1 0 0/1 2 0 0 0 0 0 0 1 0 1 0 0 0 0 0 1 - 0 1 0 0 - - 0/1 0 1 1 - - 0/1 1 - 0 0 - 0 0 - 0 0 0 0 1 0 - 3 0 ? 0 - 0 0 1 0 ? - 1 0 1 0 0 0 ? 0 1/2 - 1 0 1 0 1 0 - 1 1 2 1 0 2 - 0 0 - 0 0 0 0 0 0 0 ? 0 ? ?
7 2 2 2 1 1 1 1 2 2 1 1 ? Draft1 1 1 1 0 0 0 ? ?
2 2 2 2 1 2 1 2 Canadian Journal of Earth Sciences
5 1/2 6 1/2 1/2 1/2 1/2 1/2 ? 0 1 0 2 3 2 3 1 ? 1 0/1 1 3 1/2 1 1 - 2 - 0 - 0 - 0 - ? ? https://mc06.manuscriptcentral.com/cjes-pubs
4 0 2 1 1 0 0 ? 0 0 0 0 0 1 3 1 0 0 2 2 2 2
3 0 0 0 0 0 0 0 0 0 0 0 1 1 0 0 0 0 1 1 0 0
2 0 0 0 0 0 0 1 ? 1 0 0 0 0 1 0 1 0 0 0 0 0
0 1 0 0 0 2 0 0 0 0 2 0 0 0 0 1 1 0 0 ? 2
Taxa/character Taxa/character Charnia Trepassia Vinlandia Beothukis Avalofractus Culmofrons Pectinifrons Frondophyllas Hapsidophyllas Fractofusus andersoni Fractofusus misrai Fractofusus sp. Rangea 1 Bradgatia frond MUN Primocandelabrum Arborea Pteridinium Swartpuntia outgroup artificial holdfast outgroup artificial with