This document summarizes David Bapst's research using new approaches in phylogenetic paleobiology. It discusses using combined molecular and morphological datasets to determine which better reflects the evolutionary history of living brachiopods like rhynchonellids. It also discusses using quantitative phylogenetic methods to reconstruct relationships between direct ancestors and descendants in the fossil record, including using calibrated time-scaling and ancestor-descendant relationship inference in Cambrian trilobites. The research aims to better understand evolutionary histories and address issues like morphological convergence when using fossil data alone.

1. From Cambrian Trilobites to
Modern Brachiopods:
New Approaches in
Phylogenetic Paleobiology
David Bapst, PhD
University of California Davis

2. It All Starts With Morphology
Bapst et al., 2012, PNAS
Paleontologist relies primarily on morphology for
discriminating taxon units and inferring relationships

3. • In many groups in the fossil
record, we find specimens of
different geologic age that
share identical or very similar
morphological features
Morphology, Taxa, Trees

4. Morphology, Taxa, Trees
• In many groups in the fossil
record, we find specimens of
different geologic age that
share identical or very similar
morphological features
• We use those features to
define morphospecies
that can span millions of years,
to infer relationships among
lineages (phylogenies)

5. Systematic Paleontology
• Code taxa for discrete morphological traits (characters)
• Cladistic analyses use maximum-parsimony methods, which
attempt to find cladograms (undated trees) implying the fewest
character changes
• More generally, we refer to evolutionary trees as phylogenies,
particularly if they are dated trees
• Taxa closer together on a cladogram share more traits
~0.5 mm
MaletzandZhang,2003;C.E.Mitchell

6. Phylogenies let us Answer Questions
• When do new species or lineages first evolve?
• Which species are ancestors and which are
descendants?
• If organisms have similar morphologies, is that
similarity due to a shared evolutionary history?
• Or does shared morphology reflect similarities in
ecology and function?
These questions are key to
understanding the history of life

7. New Approaches to
Phylogenetic Paleobiology
1. Use combined molecular and
morphological datasets in living
brachiopods to determine which
dataset better reflects evolutionary
history
2. Reconstructing relationships
between direct ancestors and their
descendants across the tree of life
ImageSource:Gon,2009;S.J.Carlson

8. New Approaches to
Phylogenetic Paleobiology
1. Use combined molecular and
morphological datasets in living
brachiopods to determine which
dataset better reflects evolutionary
history
2. Reconstructing relationships
between direct ancestors and their
descendants across the tree of life
ImageSource:Gon,2009;S.J.Carlson

9. Convergence: When Morphological
Similarity Misleads Us
Maletz and Zhang, 2003
~0.5 mm
1. Combined Data Phylogenetics in Rhynchonellids

10. Mitchell, 1991
Silurian
Ordovician
~0.5 mm
1. Combined Data Phylogenetics in Rhynchonellids

11. Testing Morphological Phylogenetics
• For most fossil groups, we are forced to assume features
reflect shared evolutionary history (homology)
• Test the reliability of morphology-based phylogenies by
comparing to independent molecular data for extant taxa
• Two datasets will infer incongruent phylogenies, if one or both
datasets have poor phylogenetic signal
• A fossil-rich group with extant diversity:
• Rhynchonellida: 19 living genera (500+ extinct genera)
• Important to understand morphology to place extinct lineages
1. Combined Data Phylogenetics in Rhynchonellids

12. Rhynchonellida
• Articulated brachiopods with spirolophe lophophores
supported on crura, features of which are considered
important to systematics of the group
• 10/19 extant genera live at bathyal or abyssal depths
and are difficult to collect
Crura
Imagessource:SJCarlson
1. Combined Data Phylogenetics in Rhynchonellids

13. Hard to visualize how these differ… let’s look at tanglegrams
Note: All topologies in this section are single MPTs
or majority-rule / half-compat summaries
Morphology
(56 Characters, Reweighted Parsimony MPT)
Schreiber et al. 2013
18S and 28S rDNA
(3435 base pairs, Bayesian)
Cohen & Bitner 2013
Rhynchonellida
1. Combined Data Phylogenetics in Rhynchonellids

14. Morphology
(56 Characters, Reweighted Parsimony MPT)
Schreiber et al. 2013
18S and 28S rDNA
(3435 base pairs, Bayesian)
Cohen & Bitner 2013

15. Morphology
(56 Characters, Reweighted Parsimony MPT)
Schreiber et al. 2013
18S and 28S rDNA
(3435 base pairs, Bayesian)
Cohen & Bitner 2013
Scattered
Superfamilies

16. Why Phylogenetic Analyses Disagree
• Differences in character data used (molecular &
morphology)
• Differences in taxa included
• Differences in outgroups used for rooting
1. Combined Data Phylogenetics in Rhynchonellids

17. Outgroups Determine Where We Root Trees
• Phylogenetic analyses need to include more than just
the group of interest (the ingroup taxa)
• Need to include ‘outgroup’ taxa that are strongly
assumed to outside the ingroup to give directionality
(‘rooting’ the tree)
Mitchell et al., 2013
Outgroups
Root
Trees have no
directionality
without a root
1. Combined Data Phylogenetics in Rhynchonellids

18. Morphology
(56 Characters, Reweighted Parsimony MPT)
Schreiber et al. 2013
18S and 28S rDNA
(3435 base pairs, Bayesian)
Cohen & Bitner 2013

19. • Revise morphological data to include all
rhynchonellides that we have rDNA data for
• Use non-rhynchonellide outgroups
• Compare molecular and morphological analyses
using a standardize dataset
Bapst, Schreiber & Carlson,
in press, Syst. Biol.1. Combined Data Phylogenetics in Rhynchonellids
with Sandy Carlson
& Holly Schreiber
Is incongruence due to differences
in character data?

20. 18S and 28S rDNA
(3435 base pairs, Bayesian)
Cohen & Bitner 2013
Revised Morphological Matrix
(66 characters, Bayesian)
This Study
1. Combined Data Phylogenetics in Rhynchonellids Bapst, Schreiber & Carlson, Syst. Biol.
Inarticulate
Brachiopods
Terebratulids
Rhynch.

21. Morphology-only analyses don’t even
distinguish the rhynchonellides and the
terebratulids as separate clades
1. Combined Data Phylogenetics in Rhynchonellids Bapst, Schreiber & Carlson, Syst. Biol.
18S and 28S rDNA
(3435 base pairs, Bayesian)
Cohen & Bitner 2013
Revised Morphological Matrix
(66 characters, Bayesian)
This Study
Inarticulate
Brachiopods
Rhynch.
Terebratulids

22. • Which dataset carries the most signal of shared
evolutionary history?
• What if the two datasets both have hidden
support for a third alternative topology?
• We can answer both by combining our
morphological and molecular datasets, and
analyzing them simultaneously
Why do the datasets still disagree?
Bapst, Schreiber & Carlson,
accepted with revisions, Syst. Biol.1. Combined Data Phylogenetics in Rhynchonellids

23. Quantitative Phylogenetic Methods
• Maximum Parsimony (PAUP)
• Bayesian (MrBayes)
• Model-based phylogenetics, uses likelihood and prior
probability distributions to sample topologies via an MCMC
• Treat different data types as distinct partitions
• Same model of sequence change as Cohen & Bitner 2013
• Two morph model configurations: (1) relaxed assumptions, versus
(2) strict assumptions, to maximize information content
• Unlike maximum-parsimony which counts character changes,
Bayesian phylogenetics depend on likelihood of character
data, not directly connected to differences in # of characters
• Applied both to combined datasets, all taxa versus only
those taxa with rDNA
1. Combined Data Phylogenetics in Rhynchonellids Bapst, Schreiber & Carlson, Syst. Biol.

24. Quantitative Phylogenetic Methods
• Maximum Parsimony (PAUP)
• Bayesian (MrBayes)
• Model-based phylogenetics, uses likelihood and prior
probability distributions to sample topologies via an MCMC
• Treat different data types as distinct partitions
• Same model of sequence change as Cohen & Bitner 2013
• Two morph model configurations: (1) relaxed assumptions, versus
(2) strict assumptions, to maximize information content
• Unlike maximum-parsimony which counts character changes,
Bayesian phylogenetics depend on likelihood of character
data, not directly connected to differences in # of characters
• Applied both to combined datasets, all taxa versus only
those taxa with rDNA
1. Combined Data Phylogenetics in Rhynchonellids Bapst, Schreiber & Carlson, Syst. Biol.
…adds up to 12 analyses! How to compare?

25. Summarizing phylogenetic analyses
often results in polytomies
• When character data equally
support multiple hypotheses
of relationships, analyses
return multiple trees, which
can be very large
• Summary trees collapse those
areas of uncertainty as nodes
that aren’t fully bifurcating
• Referred to as polytomies, or
a loss of phylogenetic
resolution
Mitchelletal.,2013
1. Combined Data Phylogenetics in Rhynchonellids

26. So We Invented A New Measure…
• A measure to quantify how
different two summary trees are
• Most metrics treat polytomies
in summary trees as a
difference, even though
polytomies reflect uncertainty
• Contradiction difference (CD)
simply measures incongruence
between two summary trees
1. Combined Data Phylogenetics in Rhynchonellids Bapst, Schreiber & Carlson, Syst. Biol.

27. Pairwise Contradiction Difference
1. Combined Data Phylogenetics in Rhynchonellids Bapst, Schreiber & Carlson, Syst. Biol.
• Values at one mean trees have no similarity
• Values at zero mean trees have no disagreement

28. Pairwise Contradiction Distance
The original molecular and morphological analyses
produced completely contradictory trees
1. Combined Data Phylogenetics in Rhynchonellids Bapst, Schreiber & Carlson, Syst. Biol.

29. 18S and 28S rDNA
(3435 base pairs, Bayesian)
Reanalysis in this Study
Combined Datasets
MrBayes, Maximum Information
Shared Taxa Only
Molecular-Only Agrees With Morphology+Molecular
CD = 0.06
1. Combined Data Phylogenetics in Rhynchonellids Bapst, Schreiber & Carlson, Syst. Biol.

30. Revised Morphological Matrix
(66 characters, Bayesian)
Combined Datasets
MrBayes, Maximum Information
CD = 0.31
1. Combined Data Phylogenetics in Rhynchonellids Bapst, Schreiber & Carlson, Syst. Biol.
Morphology-Only disagrees with Morphology+Molecular

31. Poor Phylogenetic Signal of
Morphological Data Implies Convergence
• Bayesian morphological+molecular analyses were all
congruent with each other and the molecular-only tree
• Morphology-only analyses, across different methods
and sets of taxa, disagreed with each other
1. Combined Data Phylogenetics in Rhynchonellids

32. If the molecular-only and morphological+molecular
analyses are right, are there any morphological
characters that are good indicators of relatedness?
• Calculate consistency
indices for each character
• Characters that vary within
the Rhynchonellida all have
lots of convergence when
mapped on the tree from
the molecular-only analysis
• Including characters
classically used to
distinguish traditional
taxonomic groups
Classic diagnostic traits
for taxa within Rhynch.
Characters for distinguishing
articulate and inarticulate taxa
Remainder
More Informative
MissingData
1. Combined Data Phylogenetics in Rhynchonellids Bapst, Schreiber & Carlson, Syst. Biol.

33. Not the Same Story for Short-Loop Terebratulids
Molecular Only Analysis
(2574 Sites, Bayesian)
Morphology Only Analysis
(85 Characters, Bayesian)
1. Combined Data Phylogenetics in Rhynchonellids Carlson, Bapst & Schreiber, in prep.

34. Could fossil data improve
Rhynchonellide Relationships?
• Code large number of fossil taxa within Rhynchonellida to
more finely reconstruct evolutionary lineages and resolve
the appearance of convergence across modern groups
1. Combined Data Phylogenetics in Rhynchonellids Bapst, Schreiber & Carlson, Syst. Biol.
Want to read more?
This just out…

35. New Approaches to
Phylogenetic Paleobiology
1. Use combined molecular and
morphological datasets in living
brachiopods to determine which
dataset better reflects evolutionary
history
2. Reconstructing relationships
between direct ancestors and their
descendants across the tree of life
2. Ancestor-Descendants in the Fossil Record
ImageSource:Gon,2009;S.J.Carlson

36. The Question of Ancestors
in the Fossil Record
?

37. The problem is, very rarely
can we read the fossil
record as literally as this

38. How do we infer the
relationships among
ancestors & their descendants,
given the incompleteness
of the fossil record?

39. The Effects of Unsampled
Lineages In the Fossil Record
• Incompleteness of the rock record means we don’t
observe all taxa during all intervals
• Limits our ability to reconstruct precisely when lineages
originated, and what the relationships are between
morphotaxa
• Are some morphotaxa ancestral to other morphotaxa?
2. Ancestor-Descendants in the Fossil Record

40. Maletz & Mitchell (1996)
Qualitative Reconstructions
of Ancestor-Descendant
Relationships
Kennett and Srinivasan (1983)
from Pearson (1998)
2. Ancestor-Descendants in the Fossil Record

41. Inferring Ancestors in Stratocladistics
Bloch et al., 2001
2. Ancestor-Descendants in the Fossil Record
• Stratocladistic methods treat implied gaps in the fossil record as
interchangeable with morphological changes under maximum
parsimony (Fisher, 1991; 1994)
• Need formal model of diversification and incompleteness in the
fossil record to calculate likelihood of stratigraphic gap of a
given duration

42. Three-Rate Calibrated Time-Scaling (cal3)
• Takes an existing undated cladogram, sample potential
divergence dates for nodes under a likelihood function of
diversification and incompleteness of the fossil record
• Treats taxa as persistent morphotaxa, allowing for different
types of ancestor-descendant relationships based on the
overlap of their stratigraphic durations
• Created and implemented in paleotree for R (Bapst, 2012)
cal3
2. Ancestor-Descendants in the Fossil Record Bapst, 2012; Bapst, 2013; Bapst, 2014

43. ‘Budding’
Cladogenesis
Anagenesis
Modes of
Differentiation
2. Ancestor-Descendants in the Fossil Record

44. Notice that budding can
look like anagenesis
(but not vice versa)
in an incomplete record
Anagenesis
2. Ancestor-Descendants in the Fossil Record
‘Budding’

45. Ancestor-Descendant (AD) Relationships
in Cambrian pterocephaliid trilobites
• Hopkins (2011) reviewed qualitative ancestor-
descendant pairs previously suggested for this group
• Does cal3 find support for those pairs, and does it
match the mode inferred by earlier studies?
• Apply cal3 to the cladistic analysis from Hopkins (2011)
• Obtain 100 dated phylogenies, quantify support for a given
AD pair as the proportion of trees on which that pair is
inferred
Bapst & Hopkins, 2017, Paleobio.
with
Melanie
Hopkins
2. Ancestor-Descendants in the Fossil Record

46. • Each pair is a
stacked barplot
• Dots indicate
putative pairs
• Support for all
a priori AD pairs,
& a few extra
• cal3 finds very
little support for
anagenesis
• Support for budding
suggests globally
instantaneous origins
of new morphotaxa
Bapst & Hopkins, 2017, Paleobio.2. Ancestor-Descendants in the Fossil Record

47. Bayesian sampled-ancestor tip-dating
• Infer dated phylogenies from character and stratigraphic
data simultaneously in a Bayesian MCMC, under
likelihood models for morphological change and the
fossilized-birth-death model (Heath et al., 2014)
• Taxa are instantaneous points but can be placed as
sampled-ancestors (Gavryushkina et al., 2014)
Gavryushkinaetal.,2014
2. Ancestor-Descendants in the Fossil Record

48. Tip-Dating with Mesozoic Theropods
• We used a somewhat infamous dataset to compare
tip-dating methods with cal3, for ancestor-
descendant relationships, divergence dating,
estimating evolutionary rates, etc...
• Do the methods agree?
• The support for particular taxa to be probable
ancestors were fairly correlated across methods
• So… Is Archaeopteryx really the ancestral bird?
Bapst, Wright, Matzke
& Lloyd, 2016; Biol. Lett.2. Ancestor-Descendants in the Fossil Record
with
April Wright Graeme LloydNick Matzke

49. • Significant rank-order pair-
wise correlations of
ancestral placement
between methods
• Strongest between MrBayes
and BEAST2
• Considerable differences
despite similar model
• Median # of ancestors per
tree for tip-dating = 1-2
• With cal3 (using entire
taxon durations) = 17
• Always buddingBeast2
(PP)
MrBayes
(PP)
cal3
(prop)
Bapst, Wright, Matzke & Lloyd, 2016

50. Whither the Ancestral Bird?
• Archaeopteryx rarely placed as a sampled ancestor
• Never placed as ancestor on lineage leading to
extant birds, but rather as a sampled ancestor to its
sister taxon / possible synonym Wellnhoferia
Bapst, Wright, Matzke & Lloyd, 2016

51. Individual Occurrences as
Operational Taxon Units
Hunt, 2007
20 Poseidonomicus species

52. Time (Mya)
Tip-Dating Ostracod Occurrences
3 previously defined
morphospecies are
paraphyletic
(budding!)
12 sampled ancestors

53. Outgroups
MCCT
Tip-Dating with
FADs and LADs
• Ancestors among
Devonian
Terebratulide
Brachiopods?
• 9 paraphyletic
genera among 72
in-group taxa
• 21 sampled
ancestors (FADs
ancestral to
LADs)
FAD = First Appearance Datum
LAD = Last Appearance Datum

54. A New Era of Paleo-Phylogenetics
Thanks for listening! Questions?
• The rapid development and deployment of new
methods allows us to leverage phylogenies to
better understand evolution in deep time
• Bayesian phylogenetics allows us to model the
potential complexities of morphological evolution
• Methods like cal3 and tip-dating take into account
what we know about incompleteness of the rock
record, and likely existence of ancestral taxa to
create dated phylogenies from the fossil record
This research was funded by
NSF grant EAR-1147537.

56. Gaps in Densely-Sampled
Fossil Records
Maletz and Zhang, 2003; Vandenberg, 2003; C.E. Mitchell
• Closest relatives separated by a 15 to 20 million year gap in
this lineage:
• Were the intermediates living somewhere else? Open ocean?
Bergstromgraptus
Middle Darrwillian
Sinoretiograptus
Latest Katian

57. Branching Times from Time-Scaled Phylogenies
Lloyd, Bapst, Friedman
& Davis, 2016 Biol. Lett.
cal3 and a non-parametic dating method agree: accounting
for incompleteness of their records, dinosaurs likely diverged
millions of years earlier than suggested by the fossil record
2. Ancestor-Descendants in the Fossil Record