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Evolution of Shape in Diatoms
Evolution of Shape in Diatoms
Robert Bentham
Supervised by Dr Karen Page and Dr Eileen Cox
Abstract
The evolution of shape in centric diatoms is investigated by probabilistic means on phylogenetic data
using the Bayes Traits software, developed by Mark Pagel. Preliminary results of this method are presented
showing transitional rates between one trait group to another, the results suggest that diatom valve outlines
with higher degrees of symmetry are evolutionary more unstable. Weaknesses of the method used, how it
can be improved and other future possible approaches are then discussed.
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Robert Bentham: Evolution of Shape in Diatoms
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Robert Bentham: Evolution of Shape in Diatoms
structures of the ribs, which are in no way uni- phylogeny of the centric diatoms to be used and a
form across centric diatoms, on the surface of valves statistical technique for calculating the probabilis-
there are many pores. These are ofter referred to as tic rules from such a phylogeny. Ideally a phylogeny
areolae and can form intricate patterns. There can would be made specifically for this task but due to
be structures called occuli, areas where areolae are an absence of time, phylogenies from the literature
smaller and surrounded by a discrete rim of silica. will be used. This has the drawback of reducing
Additionally there can also be various elevations on the reliability of my results but the importance of
the valve, and even structures like horns. this work is to establish a framework of what can
The shape of a diatom forms during auxospore be done in the future.
development, the auxophore being the form of the The statistical analysis will be done using a piece
diatom during sexual reproduction where the cell is of software called Bayes Traits [?](software can be
roughly spherical and lacks a silica cell wall. During found at www.evolution.rdg.ac.uk) developed by
this development a complex arrangement of silica Mark Pagel.
bands and hoops form on the auxospore, this limits
its expansion and causes the distinctive shape of
many diatoms. The precise workings of this process Phylogenies
are however largely unknown making it difficult to The first phylogeny that will be used is the section
model. dealing with the centrics presented in [?] where full
details of how the phylogeny was constructed using
Valve classification the PATHd8 program [?] can be found. The data
With all these features on a centric valve, how for the phylogeny was kindly made available by Dr
exactly do you classify them into simple groups? Sorhannus in chronogram form, and can be seen in
The simplest method is to initially ignore all of the Phylogeny A.
more complicated features of diatom shape and fo- The second phylogeny used is presented in [?]
cus solely on valve outline. This is the method where full details of how the phylogeny was con-
which will be used here, though other possible tech- structed are given. Kindly Dr Theriot made the
niques will be discussed in Section 4. data available to me in phylogram form, shown in
The following classification method proposed here Phylogeny B.
is based on the symmetrical properties of the di-
atoms:
Bayes Traits
1. Contains all diatoms whose valve outlines are
circles. Bayes Traits [?] uses Markov Chain Monte Carlo
2. The bipolar diatoms, more specifically diatoms (MCMC) methods to estimate the ancestral charac-
with valve outline rotational symmetry of order ter states on phylogenies. There are different ver-
2, specifically these can be ellipses, sub-circular sions of the Bayes Traits software for continuous
or linear. and discrete traits, for our current purpose only
the method for discrete traits is of interest.
3. Diatoms with higher degrees of symmetry of
To model trait evolution, a continuous time
valve outline, includes triangular and square
Markov model is used [?], consider a binary trait
shaped diatoms.4
that can switch between two states 1 and 0 (repre-
senting say the presence or absence of a morpholog-
3 Probabilistic Rules ical feature). The rate parameters are given by q01
and q10 measuring the rate at which trait 1 changes
Now a framework will be provided showing how to trait 0 over a small time period of dt as:
the probabilistic rules of evolution of diatom shape
can be investigated. The task requires a suitable P01 (dt) = q01 dt
(1)
4
P10 (dt) = q10 dt
Diatoms with higher degrees of symmetry have been
grouped together due to their low occurence in the phyloge-
netic data, and also to increase the simplicity of the group- Over longer time periods these equations are no
ings longer valid, and the model must be written in the
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Robert Bentham: Evolution of Shape in Diatoms
Chaetoceros_calcitrans
Chaetoceros_debilis
Chaetoceros_muelleri
Chaetoceros_socialis
Chaetoceros_didymus
Chaetoceros_rostratus
Chaetoceros_sp
Eucampia_antarctica
Eucampia_zoodiacus
Lampriscus_kittonii
Toxarium_undulatum
Cyclotella_cryptica
Cyclotella_meneghiniana
Cyclotella_scaldensis
Detonula_confervacea
Thalassiosira_oceanica
Thalassiosira_pseudonana
Stephanodiscus_hantzschii
Thalassiosira_aestivalis
Thalassiosira_nordenskioeldii
Thalassiosira_angustelineata
Thalassiosira_delicatula
Thalassiosira_sp
Thalassiosira_concaviuscula
Minidiscus_trioculatus
Thalassiosira_curviseriata
Thalassiosira_profunda
Thalassiosira_tumida
Thalassiosira_eccentrica
Thalassiosira_punctigeraA
Thalassiosira_punctigeraB
Thalassiosira_rotulaCALIF
Thalassiosira_rotulaUK
Thalassiosira_minima
Planktoniella_sol
Thalassiosira_tenera
Skeletonema_grethaeATL
Skeletonema_grethaePAC
Skeletonema_pseudocostatum
Skeletonema_menzeliiA
Skeletonema_menzeliiB
Skeletonema_sp
Skeletonema_dohrnii
Skeletonema_marinoiA
Skeletonema_marinoiD
Skeletonema_marinoiC
Skeletonema_marinoiB
Skeletonema_subsalsum
Thalassiosira_guillardii
Thalassiosira_weissflogiiATL
Thalassiosira_weissflogiiIND
Lauderia_borealis
Porosira_glacialis
Porosira_pseudodenticulata
Cymatosira_belgica
Minutocellus_polymorphus
Papiliocellulus_elegans
Biddulphia_sp
Odontella_aurita
Pleurosira_laevis
Odontella_sinensis
Bellerochea_malleus
Lithodesmium_undulatum
Mediopyxis_helysia
Streptotheca_thamesis
Ditylum_brightwelli
Biddulphiopsis_titiana
Rhizosolenia_robusta
Attheya_septentrionalis
Pseudochaetoceros_sp
Gonioceros_sp
Proboscia_alata
Proboscia_indica
Actinocyclus_actinochilus
Actinocyclus_curvatulus
Actinoptychus_sinensis
Coscinodiscus_granii
Coscinodiscus_sp
Coscinodiscus_radiatus
Stellarima_microtrias
Corethron_inerme
10.0 Corethron_criophilum
Guinardia_delicatula
Rhizosolenia_setigeraD
Rhizosolenia_fallax
Rhizosolenia_shubsholei
Rhizosolenia_similoides
Rhizosolenia_imbricata
Rhizosolenia_pungens
Rhizosolenia_setigeraA
Rhizosolenia_setigeraB
Guinardia_solstherfothii
Guinardia_flaccida
Rhizosolenia_setigera
Aulacoseira_spB
Aulacoseira_crenulata
Aulacoseira_alpigena
Aulacoseira_spC
Aulacoseira_subarctica
Aulacoseira_baicalensis
Aulacoseira_islandica
Aulacoseira_skvortzowii
Aulacoseira_ambigua
Aulacoseira_valida
Aulacoseira_distans
Aulacoseira_granulataC
Aulacoseira_granulataA
Aulacoseira_granulataB
Aulacoseira_nyannensis
Aulacoseira_spA
Melosira_octogona
Melosira_varians
Podosira_stelligera
Stephanopyxis_nipponica
Stephanopyxis_palmeriana
Leptocylindrus_danicus
Leptocylindrus_minimum
Paralia_sol
Phylogeny A: Drawn with Tree View software [?], of a sample of taxa from the centric diatoms from data in [?],
used with the Bayes Traits software.
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Robert Bentham: Evolution of Shape in Diatoms
Corethron_hystrix
Stephanopyxis_turris
Aulacoseira_granulata
Melosira_nummuloides
Paralia_sulcata
Hyalodiscus_sp.
Hyalodiscus_stelliger
Rhizosolenia_setigera
Guinardia_delicatula
Rhizosolenia_imbricata
Aulacodiscus_orientalis
Aulacodiscus_sp
Actinocyclus_sp
Actinoptychus_sp.
Stellarima_microtrias
Coscinodiscus_radiatus
Coscinodiscus_wailesii
Palmeria_hardmanniana
Coscinodiscus_granii
Coscinodiscus_concinniformis
Biddulphia_tridens
Attheya_septentrionalis
Biddulphia_alterans
Chrysanthemodiscus_sp
Trigonium_formosum
Biddulphiopsis_membranacea
Biddulphiopsis_titiana
Isthmia_enervis
Lampriscus_orbiculatum
Lampriscus_shadboltianum
Toxarium_undulatum
Toxarium_hennedyanum
Ardissonea_sp.
Climacosphenia_sp.
Ardissonea_formosum
Brockmanniella_brockmannii
Campylosira_cymbelliformis
Leyanella_arenaria
Extubocellulus_cribriger
Papiliocellulus_simplex
Arcocellulus_mammifer
Minutocellus_polymorphus
Cerataulina_pelagica
Terpsinoe_musica
Hydrosera_sp
Urosolenia_eriensis
Acanthoceros_sp.
Hemiaulus_sinensis
Chaetoceros_muelleri
Chaetoceros_peruvianus
Odontella_sinensis
Mastodiscus_radiatus
Amphitetras_antediluvianum
Pleurosira_laevis
Odontella_cf._aurita_23vi081ACX
Odontella_cf._aurita_26VI083DCX
Odontella_cf._aurita_26vi081LCX
Cerataulus_smithii
Triceratium_sp
Triceratium_dubium
Triceratium_cf._dubium
Bellerochea_horologicalis
Lithodesmioides_polymorpha
Lithodesmium_undulatum
Lithodesmium_intricatum
Lithodesmium_sp
Porosira_glacialis
Cyclotella_meneghiniana
Thalassiosira_pseudonana
Planktoniella_sol
Cyclostephanos_dubius
Cyclotella_sp.
Detonula_confervacea
Minidiscus_trioculatus
Bolidomonas_pacifica
0.05
Phylogeny B: Drawn with Figtree software, of a sample of taxa from the centric diatoms from data in [?]. Branches
are colour coded representing the trait group. Green refers to group 1, red group 2 and blue group 3.
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Robert Bentham: Evolution of Shape in Diatoms
Phy Prior q12 : Av q12 :Var q13 :Av q13 :Var q21 :Av q21 :Var
A Uniform 13.60 44.87 3.602 8.569 63.39 608.6081
B Uniform 1.250 0.7760 1.927 8.541 2.496 3.015
B hyperprior exp 0.8928 0.5063 0.8716 0.9081 3.216 2.247
Phy Prior q23 : Av q23 : Var q31 :Av q31 :Var q31 :Av q32 :Var
A Uniform 20.6081 310.4 67.77 597.8 65.95 642.7
B Uniform 5.476 29.54 18.96 180.0 13.67 201.4
B hyperprior exp 3.283 3.216 11.07 46.03 6.157 26.82
Table 1: Average and Variance of the rate parameters from Bayes Traits analysis using phylogenies A and B and
prior distributions. The prior was originally chosen as a uniform distribution between 0 and 100 for both phylogenies.
With this, Phylogeny A gave poor results with very high variances. With the uniform prior for phylogeny B the
results are better with smaller variances, but still become quite large. Since the number of species listed in the
phylogeny is small and only 75, a uniform distribution is most likely not suited as a prior and a properly chosen
stronger prior should be used. For the rate parameters, we know that they must be positive, and they are not
expected to be very large, thus an exponential distribution should fit. To avoid the difficulty of choosing the right
parameters for this exponential function, the mean of the exponential is seeded with a uniform distribution known
as a hyperprior. The ancestral state of the root node though calculated has been omitted from the table. This is
due to the pennate branch of diatoms being absent from the phylogeny and hence any result not being reliable.
Attheya even have horns. Thus dividing diatoms fine a simple closed curve. This technique has al-
shape into three classes does not nearly represent ready been applied to diatoms, in [?] the first 30
features that have evolved and this simplistic anal- fourier descriptors were used to describe the valve
ysis needs to be extended to provide deeper insight. shape. Due to the high number of parameters of
Here two possible methods will be described in de- this new data set [?] uses principle component anal-
tail. ysis (PCA) to reduce the dimensionality and clas-
sify the diatoms into groups.
Once fourier descriptors have been obtained either
Method 1.-Single genus phylogenies
PCA could be used to classify the diatoms into dis-
To fully describe the variety of forms of diatom crete groups then the Bayes Traits analysis could
shape more classification groups which are more be run as previously, or the continuous model of
specific are needed. However there is a limit on Bayes Traits could be used. The continuous model
how many groups are used, due to enough taxa be- uses a constant but unknown variance random walk
ing required in each group for meaningful statistical (brownian motion) model and is described in detail
results. Instead of creating very large phylogenies in [?], a generalised least square (GLS) approach is
over all the genera of diatoms, it should be possible used to estimate the trait value of each species t 2
to focus on only one smaller branch. This would where t is the path length to the root of the tree
give a detailed account of evolution and could be and 2 is the variance. There are other continuous
used to show how features like sectors have evolved quantities besides fourier descriptors which can be
in genera such as Asterophalus. used, for instance [?] shows how the curvature of a
diatom valve can be obtained and thus be used to
distinguish diatoms.
Method 2.- Continuous models
Instead of using discrete classification groups of
Other possible models
traits, a continuous measure of traits could be
used. One way of achieving this would be by using The continuous markov model used previously
Fourier Descriptors. Fourier descriptors are fully may not be the best model to use to explain di-
described in [?] and in brief are a set of numbers atom shape evolution, due to the assumptions it
obtained from a Fourier series that completely de- makes. While certainly useful in many cases, other
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Robert Bentham: Evolution of Shape in Diatoms
models could be created that may also be useful in phological feature and others like it that cause un-
gaining insight. Features such as valve outline for expected evolutionary results can not be expressed
the pennates seem to change little in [?] the exact in a model that switches between a limited set of
nature of morphological change over the geological traits. Novel features in diatoms could evolve like
range of the diatom Nitzschia jouseae was found to the raphe as an advantageous new form of locomo-
be of evolutionary stasis. This suggests that high tion or as causing some other beneficial interaction
degrees of morphogenetic stability can exist in the in their environment such as with a certain kind
diatom taxa, which are not represented in a contin- of bacteria. This provides much difficulty for how
uous markov model. exactly can you predict and model the evolution of
Alternatively an evolutionary model of diatom such novel unexpected traits without knowing the
shape could be constructed. The genome would be full details a priori?
represented by a set of fourier descriptors for the What this short work hopefully has shown is the
outline of the diatom at various heights, in a way potential to use various mathematical techniques
that would describe its entire 3D shape. Mutations to investigate this problem. In a brief period of
in the genome will correspond to shape changes, time the result was obtained that valves with higher
and with a suitably chosen fitness function the evo- degrees of symmetry statistically are most unstable,
lution of the shape could be studied over genera- while this result is not as statistically rigorous as
tions. The choice of the fitness function here is key, would be liked, it shows the direction future work
it is difficult to imagine such a simple mathemati- can and hopefully will head in.
cal function that would reproduce all the complex-
ities seen in diatom structure, but a basic function
containing various physical constraints and possi-
Acknowledgements
ble interactions with bacteria would be interesting Thanks to Dr. Ulf Sorhannus and Dr. Edward
to examine. Theriot for kindly sharing their phylogenetic data
with me in NEWICK format and thus saving me
a substantial amount of time. Special thanks also
5 Final Discussion to my supervisors Dr. Karen Page and Dr. Eileen
There is much more work to do on the study of the Cox for their help throughout.
evolution of diatom shape, the controlling feature
of determining the form of the silica shell is genetic, References
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