Marine Animals
I. The Invertebrates
OCN 201 Biology Lecture 7
Illustration : Ernst Haeckel
Arthropods
The Animal
Family Tree
Segmented
Worms
Vertebrates
Mollusks
Echinoderms
Round Worms
40 animal phyla
Cnidarians
Ctenophores
Sponges
Rad
a
eri
at
Bil
32 phyla are
multicellular
invertebrates
iata
Flatworms
No symmetry
Placozoa
Ancestral
Protist
ctenophores
Wnt/Wg
13 DECEMBER 2013
Ctenophores
Sponges
Noggin
Mef2
Ctenophora
Gli
a
eri
at
Bil
Rad
iata
VOL 342
NK2
Eomes
Porifera
Slp
Eya
Mrf4
MyoG
Six1/4
Arthropods
NK4
Placozoa
Ancestral
Protist
www.sciencemag.org
Bilateria
SCIENCE
1242592-4
No symmetry
VOL 342
The list of author affiliations is available in the full article online.
*Corresponding author. E-mail: [email protected]
The Animal
Family Tree
(Cn,Ct)
Bi B
Cn
Ct
Tr
Po
(Ct,Bi)
Bi C
Ct
Cn
Tr
Po
(Po,)
Bi D
Cn
Tr
Ct
Po
(Ct,)
Bi E
Cn
Tr
Po
Ct
(Tr,)
Fig. 3. Tree produced by maximum-likelihood
Ephydatia muelleri
analysis
of the EST set.
96
Cyanea capillata
Fig. 4. Tree produced by maximum-likelihood
Clytia hemisphaerica
analysis of gene content.
Hydra magnipapillata
Bi F
Cn
Ct
Po
Tr
(Bi,)
Bi
Cn
Ct
Po
Tr
Later development of M. leidyi embryo shown oral side down. Embryos are about
200 mm. See the supplementary materials for a more detailed description of the
ctenophore body plan. [Photo credit for (A): courtesy of Bruno Vellutini]
SCIENCE
Myf5 MyoD
Vertebrates
Trichoplax adhaerens
Placozoa
Cnidaria
Shh/hh
Fig. 3. Tree produced by maximum-likelihood analysis of the EST Set. The tree was produced from a matrix consisting of 242 genes and 104,840 amino
FGF
acid Cnidaria
characters. Circles on nodes C
indicate 100% bootstrap
support. Support
placing ctenophores as sister to the rest of Metazoa is 96% of 100 bootstrap
BMPs/dpp
replicates.
Twist
GATA
www.sciencemag.org
NK3
Snail
Lbx
Segmented
Worms
13 DECEMBER 2013 VOL 342 SCIENCE www.sciencemag.org
Published by AAAS
Mollusks
Echinoderms
Round Worms
Cnidarians
Text
Flatworms
www.sciencemag.org
Porifera
SCIENCE
Ctenophora
VOL 342
Rhizopus orizae
13 DECEMBER 2013
Amoebidium
Cite this article as
J. F. Ryan etparasiticum
al.,
Sphaeroforma arctica
Science 342, 1242592 (2013).
Capsaspora_owczarzaki
DOI: 10.1126/science.1242592
Monosiga ovata
1242592-2
groups with non-ctenophores. The average length
of an unspliced M. leidyi transcript is 5.8 kb. Eight
percent of predicted genes are embedded within
other genes. This number of nested intronic genes
is high compared to other genomes (table S2), but
may be inflated owing to a subset of these being
alternatively expressed exons. The level of repetitive sequence in the M. leidyi genome is low to
moderate, as compared to other metazoans (tables
S3 and S4); this has made it possible to produce a
high-quality genome assembly based on pairedend and mate-pair sequencing alone. Additional
characteristics of this genome are presented in
tables S5 to S10.
Cryptococcus neoformans
READ THE FULL ARTICLE ONLINE
Phycomyces blakesleeanus
http://dx.doi.org/10.1126/science.1242592
Bilateria
Characteristics of the M. leidyi Genome
The M. leidyi genome is among the smallest 7%
of genomes when compared with those cataloged
in the Animal Genome Size Database (26) and is
densely packed with gene sequences. It encodes
16,548 predicted protein-coding loci, which make
up 58% of the genome, and we conservatively assign 44% of these gene predictions into homology
as determined by baa.pl (25), was 98.2%. In
94.8% of cases, a single EST mapped completely
to a single scaffold. These numbers suggest that
the assembly is both complete and accurately
assembled.
Arthropods
Spizellomyces punctatus
Batrachochytrium dendrobatidis
Phylogenetic Position of M. leidyi
The availability of the complete genome of M. leidyi
has allowed us to improve on the ctenophore
sampling used in previous phylogenomic analyses
of gene sequence evolution. We assessed two data
matrices that differ in breadth of taxon sampling
and fraction of missing data: a “Genome Set” that
includes only data from complete genomes (13 animals, 19.6% missing data) and an “EST Set” that
includes partial genomic data from many taxa (58
animals, 64.9% missing data). We analyzed both
matrices by using maximum-likelihood [with the
GTR+G model as implemented in RAxML (27)]
and Bayesian [with the CAT model as implemented
in PhyloBayes (28)] methods. To understand the
effect of outgroup selection on our ingroup topology, we included four different sets of nonmetazoan
outgroups (table S11) in each combination of method and matrix. This multifactorial strategy yielded
a total of 16 analyses (Table 1).
We found no support in any of these analyses
for Coelenterata (Cn,Ct), Diploblastica (Bi,), or
Placozoa being the sister lineage to the rest of
animals (Tr,) (Table 1 and fig. S1). We recovered
broad support for a sister relationship between
Cnidaria and Bilateria (Cn,Bi) and for a clade
of Placozoa, Cnidaria, and Bilateria (Tr,Cn,Bi).
Maximum-likelihood analyses support the placement of Ctenophora as sister group to all other
Salpingoeca rosetta
Monosiga brevicollis
Pleurobrachia pileus
Mnemiopsis leidyi
Mertensiid sp
Leucetta chagosensis
FIGURES IN THE FULL ARTICLE
Sycon raphanus
88
Oscarella carmela
Fig. 1. M. leidyi life history and anatomy.
Oscarella lobularis
77
Oopsacas minuta
Fig. 2. Previously
proposed relationships
Carteriospongia foliascens
98
Amphimedon queenslandica
97
of the five deep
clades of animals.
Suberites domuncula
96
Lubomirskia baicalensis
Fig. 2. Previously proposed relationships of the five deep clades of animals. The label at the
bottom of each pane corresponds to the header of Table 1. (A) Coelenterata hypothesis. (B) Ctenophora as
sister to Bilateria. (C) Porifera as sister group to the rest of Metazoa. (D) Ctenophora as sister group to the
rest of Metazoa. (E) Placozoa as sister group to the rest of Metazoa. (F) Diploblastica hypothesis. We see no
support in any of our analyses for the hypotheses in (A), (E), and (F) and very little support for (B) (see
Table 1). Ct, Ctenophora; Po, Porifera; Tr, Placozoa; Cn, Cnidaria; Bi, Bilateria.
A
96
13 DECEMBER 2013
Placozoa
nu
cle
us
Podocoryna carnea
Fig. 5. The origin of postsynaptic genes.Hydractinia echinata
Nematostella vectensis
82
Anemonia
viridis
Fig. 6. Inventory of myogenic components
Aiptasia pallida
in M. leidyi.
Metridium senile
Methods: We have sequenced, annotated, and analyzed the 150-megabase genome of the ctenoAcropora palmata
Acropora millepora
phore Mnemiopsis leidyi. We have performed detailed phylogenetic analyses on these new data SUPPLEMENTARY MATERIALS Porites
astreoides
Montastraea faveolata
using both sequence matrices and information on gene content. We conducted extensive genomic
Xenoturbella bocki
Materials
and
Methods
inventories on signaling pathway components and genes known to be critical to neural and mesoNemertoderma westbladi
45
Figs. S1 to S10
Meara stichopi
dermal cell types, among others.
Isodiametra pulchra
Tables S1 to S31 98
Symsagittifera roscoffensis
Results: Our phylogenetic analyses suggest that ctenophores are the sister group to the rest of the References
Convolutriloba longifissura
extant animals. We find that the sets of neural components present in the genomes of Mnemiopsis
Saccoglossus kowalevskii
Ptychodera flava
and the sponge Amphimedon queenslandica are quite similar, suggesting that sponges have the
Strongylocentrotus purpuratus
necessary genetic machinery for a functioning nervous system but may have lost these cell types.
Asterina pectinifera
44
Branchiostoma floridae
We also find that, although Mnemiopsis has most of the genes coding for structural components of
Petromyzon marinus
83
mesodermal cells, they lack many of the genes involved in bilaterian mesodermal specifi
cation and,
Gallus gallus
= 100 bootstrap
Ciona intestinalis
therefore, may have independently evolved these cell types.
support
Halocynthia roretzi
The phylogenetic
position of the ctenophore
43
Echinoderes horni
Discussion: These results present a newly supported view of early animal evolution that accounts Mnemiopsis leidyi and88its implications regarding
Xiphinema index
94
Euperipatoides
kanangrensis
the origin of mesodermal cell types. (A) Adult
for major losses and/or gains of sophisticated cell types, including nerve and muscle cells. This
0.2
Anoplodactylus
eroticus
99 relationships of the five
evolutionary framework, along with the comprehensive genomic resources made available through M. leidyi. (B) Summary99of the
Boophilus microplus
main
branches
of
animals
and
the
outgroup
ChoanoDaphnia
pulex
this study, will yield myriad discoveries about our most distant animal relatives, many of which will
93
Drosophila melanogaster
flagellata. (C) Inventory
of myogenic specification
shed light not only on the biology of these extant organisms but also on the evolutionary history of genes in Mnemiopsis. Components present in the
Schmidtea mediterranea
Paraplanocera oligoglena
all animal species, including our own.
Mnemiopsis genome
are in blue, and names
aretelata
Capitella
95
underlined. Absent components are in red. The lack of Helobdella robusta
84 in Mnemiopsis indicates
Cerebratulus
many of these factors
that lacteus
85
Terebratalia transversa
ctenophore mesodermal
44cell types are specified differEuprymna scolopes
ently than in bilaterians, suggesting that they Lottia
perhaps
gigantea
evolved independently in these two lineages. Crassostrea virginica
Fig. 1. M. leidyi life history and anatomy. (A) Adult M. leidyi (about 10 cm
long). (B) Close-up view of comb rows. (C) Aboral view of cydippid stage. (D) Onecelled fertilized embryo. (E to H) Early cleavage stages. (I) Gastrula stage. (J to M)
Vertebrates
1242592-2
Choanoflagellata
Bi
Cn
Ct
Po
Tr
B
Bi F
Cn
Ct
Po
Tr
(Science 2013)
Bi E
Cn
Tr
Po
Ct
Introduction: An understanding of ctenophore biology is critical for reconstructing events that
occurred early in animal evolution. The phylogenetic relationship of ctenophores (comb jellies) to
other animals has been a source of long-standing debate. Until recently, it was thought that Porifera (sponges) was the earliest diverging animal lineage, but recent reports have instead suggested
Ctenophora as the earliest diverging animal lineage. Because ctenophores share some of the same
complex cell types with bilaterians (such as neural and mesodermal cells), the phylogenetic position
of ctenophores affects how we think about the early evolution of these cell types.
Bi D
Cn
Tr
Ct
Po
Joseph F. Ryan, Kevin Pang, Christine E. Schnitzler, Anh-Dao Nguyen, R. Travis Moreland,
David K. Simmons, Bernard J. Koch, Warren R. Francis, Paul Havlak,
NISC Comparative Sequencing Program, Stephen A. Smith, Nicholas H. Putnam,
Steven H. D. Haddock, Casey W. Dunn, Tyra G. Wolfsberg, James C. Mullikin,
Mark Q. Martindale, Andreas D. Baxevanis*
Bi C
Ct
Cn
Tr
Po
72
Bi B
Cn
Ct
Tr
Po
The Genome of the Ctenophore
Mnemiopsis leidyi and Its Implications
for Cell Type Evolution
A
RESEARCH ARTICLE
Phylogenetic Position of M. leidyi
The availability of the complete genome of M. leidyi
has allowed us to improve on the ctenophore
sampling used in previous phylogenomic analyses
of gene sequence evolution. We assessed two data
matrices that differ in breadth of taxon sampling
(Bi,)
(Tr,)
(Ct,)
(Po,)
(Ct,Bi)
(Cn,Ct)
and fraction of missing data: a “Genome Set” that
includes only data from complete genomes (13 aniFig. 2. Previously proposed relationships of the five deep clades of animals. The label at the
mals, 19.6% missing data) and an “EST Set” that
as
Ctenophora
(B)
hypothesis.
Coelenterata
(A)
1.
Table
of
header
the
to
corresponds
bottom of each pane
genomic data from many taxa (58
sister to Bilateria. (C) Porifera as sister group to the rest of Metazoa. (D) Ctenophora as sister group to the includes partial
data). We analyzed both
rest of Metazoa. (E) Placozoa as sister group to the rest of Metazoa. (F) Diploblastica hypothesis. We see no animals, 64.9% missing
(see
(B)
for
support
little
matrices by using maximum-likelihood [with the
very
and
(F)
and
(E),
(A),
in
hypotheses
the
for
analyses
our
of
support in any
GTR+G model as implemented in RAxML (27)]
Table 1). Ct, Ctenophora; Po, Porifera; Tr, Placozoa; Cn, Cnidaria; Bi, Bilateria.
and Bayesian [with the CAT model as implemented
in PhyloBayes (28)] methods. To understand the
outgroup selection on our ingroup topolas determined by baa.pl (25), was 98.2%. In groups with non-ctenophores. The average length effect of
included four different sets of nonmetazoan
94.8% of cases, a single EST mapped completely of an unspliced M. leidyi transcript is 5.8 kb. Eight ogy, we
(table S11) in each combination of methto a single scaffold. These numbers suggest that percent of predicted genes are embedded within outgroups
matrix. This multifactorial strategy yielded
the assembly is both complete and accurately other genes. This number of nested intronic genes od and
is high compared to other genomes (table S2), but a total of 16 analyses (Table 1).
assembled.
We found no support in any of these analyses
may be inflated owing to a subset of these being
alternatively expressed exons. The level of repeti- for Coelenterata (Cn,Ct), Diploblastica (Bi,), or
Characteristics of the M. leidyi Genome
being the sister lineage to the rest of
The M. leidyi genome is among the smallest 7% tive sequence in the M. leidyi genome is low to Placozoa
(Tr,) (Table 1 and fig. S1). We recovered
of genomes when compared with those cataloged moderate, as compared to other metazoans (tables animals
support for a sister relationship between
in the Animal Genome Size Database (26) and is S3 and S4); this has made it possible to produce a broad
and Bilateria (Cn,Bi) and for a clade
densely packed with gene sequences. It encodes high-quality genome assembly based on paired- Cnidaria
Cnidaria, and Bilateria (Tr,Cn,Bi).
16,548 predicted protein-coding loci, which make end and mate-pair sequencing alone. Additional of Placozoa,
analyses support the placeMaximum-likelihood
in
presented
are
genome
this
up 58% of the genome, and we conservatively as- characteristics of
ment of Ctenophora as sister group to all other
sign 44% of these gene predictions into homology tables S5 to S10.
Later development of M. leidyi embryo shown oral side down. Embryos are about
200 mm. See the supplementary materials for a more detailed description of the
ctenophore body plan. [Photo credit for (A): courtesy of Bruno Vellutini]
A
Fig. 1. M. leidyi life history and anatomy. (A) Adult M. leidyi (about 10 cm
long). (B) Close-up view of comb rows. (C) Aboral view of cydippid stage. (D) Onecelled fertilized embryo. (E to H) Early cleavage stages. (I) Gastrula stage. (J to M)
1336
RESEARCH ARTICLE
RESEARCH ARTICLE
RESEARCH ARTICLE SUMMARY
Segmented
Worms
Saccharomyces cerevisiae
Outgroup
Invertebrate Phyla
• Placozoa
• Porifera (sponges)
• Cnidarians (jellyfish, corals, hydroids)
• Ctenophores (comb jellies)
• Flat Worms
• Round Worms
• Molluscs (clams, snails, squid, octopi)
• Segmented Worms
• Arthropods (copepods, crabs, shrimp)
• Echinoderms (sea stars, brittle stars)
Placozoa
• Simplest animal?
• Lacks symmetry
• Only four cell types
• No tissues or organs
• Found on surfaces
• Probably feeds on surface algae and bacteria
• Can fold itself to create a digestive pocket
Porifera
(sponges)
• “Skeleton” may be calcareous or silica
spicules, or entirely of the protein collagen
• Benthic -- intertidal to abyssal, all latitudes
Feeders (feeding on plankton,
• Suspension
bacteria. A few exceptions)
• Large range of cell types, lack of tissue types
• Source of many bioactive compounds
Diversity in size & shape,
Many growth forms
MBARI
Sponge Skeletons
Natural Sponge
Glass sponge
( Venus’ Flower
Calcareous Sponge
Basket)
collagen
Sponge Anatomy
choanocyte
Arthropods
The Animal
Family Tree
Vertebrates
Segmented
Worms
Mollusks
Echinoderms
Round Worms
Cnidarians
ate
Bil
Sponges
Rad
ria
Ctenophores
iata
Placozoa
Ancestral
Protist
Ctenophores
(comb jellies)
Flatworms
Ctenophores
(comb jellies)
• Have eight rows of cilia (comb rows)
• Carnivorous
• Use tentacles with sticky colloblasts
• Some directly ingest prey (Beroe)
• Can be invasive (e.g., Black Sea)
RESEARCH ARTICLE
lobate
cestid
beroe
cydippid
Fig. 1. M. leidyi life history and anatomy. (A) Adult M. leidyi (about 10 cm
pid stage. (D) One-
Later development of M. leidyi embryo shown oral side down. Embryos are about
200 mm. See the supplementary materials for a more detailed description of the
• All are marine
from 0 to >3000 m (few benthic
• Pelagic
creepers)
Cnidarians
(anemones, corals, jellyfish)
• Named for the stinging cells (cnidocytes)
• Radial symmetry
• Two forms: polyps and medusae
• Asexual and Sexual Reproduction
•
•
Radial symmetry
•
No circulatory,
respiratory or
excretory systems
•
•
Simple Digestive system
(blind sac)
carnivores/detritovores
Primitive nerve
networks
Polyp Medusa
Cnidocytes
Cnidocytes
• Prey capture
• Turf wars
• Defense
toxins
Class Hydrozoa: hydroids and hydromedusae
Class Anthozoa: Sea anenomes, corals, sea pens
Class Cubozoa: sea wasps and box jellies
Class Scyphozoa: jellyfish (big jellies)
Jellyfish and fisheries
Arthropods
The Animal
Family Tree
Vertebrates
Segmented
Worms
Mollusks
Echinoderms
Round Worms
Cnidarians
Sponges
Rad
a
eri
at
Bil
Ctenophores
iata
Placozoa
Ancestral
Protist
Flatworms
Flatworms
(Platyhelminthes)
• Turbellarian flatworms are marine, benthic
• Infauna from intertidal to deep sea
• Carnivorous or herbivorous
• Move by cilia or undulations
• Mouth but no anus
• Cephalization
Roundworms
(Nematodes)
• Flow-through digestive system!
• Found all over (terrestrial, freshwater, marine)
• VERY abundant free-living in benthic infauna
• Many other types are parasitic
• Many are deposit feeders, detritivores
Arthropods
The Animal
Family Tree
Vertebrates
Segmented
Worms
Mollusks
Echinoderms
Round Worms
Cnidarians
ate
Bil
ria
Ctenophores
Rad
iata
Sponges
Placozoa
Ancestral
Protist
Molluscs
MAJOR CLASSES
• Bivalvia (Clams, oysters, mussels)
• Gastropoda (snails, nudibranchs)
• Cephalopoda (squid, octupus, nautilus)
Flatworms
Bivalves
Burrowing
• Many burrowing and boring boring
• Others attach to rocky surfaces
• Suspension feeding or selective deposit feeding
Gastropods
•
Many with shells (snails, whelks, etc.) some
types without shells (e.g. nudibranchs)
•
•
Some planktonic forms (e.g. pteropods)
•
Have a radula (a toothed scraper)
Herbivores and carnivores, deposit and
suspension feeders
Cephalopods
•
•
•
•
•
Well developed brains and eyes
Many have ink sacs
Only one type still has external shell (Chambered
nautilus)
Carnivores; Use radula and beak for tearing food
Many can rapidly change colors (camouflage,
communication)
Arthropods
The Animal
Family Tree
Vertebrates
Segmented
Worms
Mollusks
Echinoderms
Round Worms
Cnidarians
Sponges
Rad
a
eri
at
Bil
Ctenophores
iata
Placozoa
Ancestral
Protist
Flatworms
Segmented Worms
(Annelids)
• Major Class: the Polychaetes
• Mostly benthic, a few planktonic
- predatory epifauna
- tube-dwelling infauna (deposit/
suspension feeders)
well developed
central nervous
system
Polychaetes
Food capture & Gas Exchange
Christmas
tree worm
tube dwelling
Arthropoda
(jointed feet)
•
•
•
•
Exoskeleton (protection, leverage)
Striated Muscle (quick, powerful)
External Skeleton requires molting
Herbivores, carnivores, omnivores
Arthropoda: Crustacea
Malacostraca
branchiopods
ostracods
isopods
copepods
amphipods
mysids
decapod
Arthropoda
•
•
Vast majority of marine arthropods are crustaceans
Exceptions: marine insects, chelicerates (e.g., horseshoe
crabs, pycnogonids)
horseshoe crabs
halobates
Arthropods
The Animal
Family Tree
Vertebrates
Segmented
Worms
Mollusks
Echinoderms
Round Worms
Cnidarians
Bil
Sponges
Rad
ria
ate
Ctenophores
iata
Placozoa
Ancestral
Protist
Flatworms
Echinoderms
• Echino derm = spiny skin
are suspension or deposit feeders,
• Most
some grazers (e.g., kelp), sea stars also
predatory
• From intertidal to abyssal depths, benthic,
often have planktonic larvae
• Have tube feet
symmetric as larvae, adults
• Bilaterally
pentaradially symmetric
Echinoderms
Sea Stars
Sea Cucumbers
Sea Urchins
Brittle Stars
tube feet
Crinoids
Echinoderms
Questions?