Transcript Lecture 11, lophophorates, revised - Cal State LA

Lophophorates – a clade, or not?
Once upon a time, there were 3 phyla that had an apparent
synapomorphy: the lophophore, a horseshoe-shaped ring
of ciliated tentacles surrounding mouth, used in filter feeding
Phylum Bryozoa
- colonies made of
microscopic zooids
Phylum Phoronida
- worm-like, tube-dwelling; large
Phylum Brachiopoda
- 2 shell valves; large
Lophophorates on the Tree of Life
Lophophorates were 1st placed in the Deuterostomia, as:
- their early embryonic cleavage is radial & indeterminate
- body forms with 3 regions and a 3-part coelom
However, they also share some protostome characteristics:
- mouth develops from blastopore in one group, Phoronids
- larvae of some look like modified trochophores
- they can make chitin, a building material not found in
Deuterostomia
Where does molecular analysis of DNA + protein sequence
data place them...?
Tree #1:
early 1990s
Annelids
OLD
SCHOOL
PHYLOGENY
Arthropods
Molluscs
(wrong)
Protostomes
Nematodes
Platyhelminthes
Lophophorates
Deuterostomes
Tree #2:
1995
DNA analysis: Lophos = protostomes
Comparison of the highly-conserved
18S rRNA gene sequence showed
that all 3 lophophorates grouped
with protostomes, not with the
deuterostomes
Proposed clade within protostomes:
the Lophotrochozoa
- lophophorates, molluscs + annelids;
either have a lophophore, or a
trochophore larva (no real
synapomorphy; not legit for a name)
Halanych et al. 1995
arthropods + nematodes are in a
separate clade, Ecdysozoa
Protostomes
Lophotrochozoa
Two distinct clades within
protostomes... but in which
do the lophophorates belong?
Nematodes
Arthropods
Ecdysozoa –
molting phyla
Deuterostomes
Phoronids
Lophotrochozoa
Chaetognaths
Brachipoda
Nemertea
Mollusca
Annelida
Platyhelminthes
Trochozoa
phyla with a
trochophore
larval stage
Platyzoa
Rotifera
Bryozoans
Tree #3:
2009
Entoprocts
Cycliophorans
- analysis of 1,487 genes
Polyzoa
Phoronids
Chaetognaths
Brachipoda
Nemertea
Mollusca
Annelida
The former
“lophophorates”
are scattered
among all the
major clades
 so... not a
monophyletic
group (in 2009)
Platyhelminthes
Rotifera
Bryozoans
Entoprocts
Tree #3
Cycliophorans
- analysis of 1,487 genes; Hejnol et al. 2009, Proc Roy Soc B
Phoronids
Chaetognaths
Brachipoda
Nemertea
Mollusca
Annelida
The former
“lophophorates”
are scattered
among all the
major clades
 implies that the
lophophore evolved
multiple times
Platyhelminthes
Rotifera
Bryozoans
Entoprocts
Tree #3
Cycliophorans
- analysis of 1,487 genes; Hejnol et al. 2009, Proc Roy Soc B
Tree #4
- analysis of >72,000 amino acid positions
Platyhelminthes
Mollusca
Annelida
Nemertea
(ribbon worms)
new Lophophorata?
suggests the
lophophore really
is a synapomorphy
and Lophophorata
is monophyletic!..
..if you now include
the entoprocts
Brachiopoda
Phoronida
Bryozoa
Entoprocta
Laumer et al. 2015, Current Biology
Polyzoa
Lophophorate characteristics
Body divided in 3 parts, each with its own coelomic space:
Anterior
Posterior
Coelomic space
Protocoel
Body region
Prosome
Mesocoel
Mesosome
Metacoel
Metasome
This 3-part body/coelom structure is typical of deuterostomes
like us... probably an ancestral feature kept by deuterostomes
and lophophorates, which changed in other trochozoans like
molluscs and annelids
The Lophophore
3 phyla have a lophophore,
a circle of tentacles used
in suspension feeding
Ciliated growth of tentacles arising
from mesosome (middle coelomic
compartment)
- tentacles contain fingers of coelom
- surround mouth, but not anus
Lophophore Function
Cilia on lophophore tentacles generate a feeding current
- cilia catch particles, bounce them back and forth to mouth
- each tentacle has 1 row of frontal
cilia and 2 rows of lateral cilia
Phylum Bryozoa
5,000 spp.
- Prosome reduced/absent; mesosome fills lophophore +
connects to metasome, which contains viscera (organs)
- Colonial, made up of individual zooids that bud asexually
- zooids bilaterally symmetric, often polymorphic
- U-shaped gut, anus outside lophophore
- No excretory or circulatory systems; whole body of an
individual zooid may be reduced to “brown body” + excreted
- Hermaphrodites, as a colony; gonads simple, temporary
- Undergo radial cleavage (like deuterostomes);
blastopore does not become mouth or anus (unique to them)
- Most produce lecithotrophic larvae that settle rapidly;
important members of fouling communities
Polypide = soft tissue + lophophore
Zooid = exoskeleton + polypide
Autozooids = feeding
Heterozooids = no lophophore,
do other functions for colony
Compare & contrast bryozoans
with hydrozoans (Cnidaria) –
What convergent adaptations for
colonial life do the 2 groups show?
Heterozooids = no lophophore,
do other functions for colony
Ovicells – incubators for developing embryos
- sperm taken up from seawater, used to fertilize eggs
- parental zooid degenerates, forming nutritive tissue
chamber for fertilized eggs
Avicularia – giant claws used to defend colony
- polypide reduced to a few large muscles
- claw is modified operculum
- prevents fouling by larvae + spores of other organisms
swimming
larva
colony of
inter-connected
zooids
ancestrula
asexual
reproduction
- Colony starts as a metamorphosed larva, which grows into
one original zooid, the ancestrula
- ancestrula then clones itself to form whole colony, asexually
Bryozoan Groups
Class Stenolaemata (tubular; mostly extinct)
Class Gymnolaemata
- zooids connected by funiculus (a coelomic link)
Order Cheilostomata
- openings covered by opercula
- embryos usually brooded in ovicells
- avicularia: claws function in defense
Order Ctenostomata
- cylindrical zooids, attached by stolon
- no operculum, ovicells or avicularia
Class Gymnolaemata
Order Ctenostomata
- cylindrical zooids
- flexible, chitinous
exoskeleton
- zooids sprout from
a horizontal runner
called the stolon
(at some distance from
each other)
Funiculus = coelomic
connection between zooids
(may even link stomachs)
funiculus
Class Gymnolaemata
Order Ctenostomata
Extend lophophore by hydrostatic pressure:
- parietal muscles contract, pressurizing coelom
- fluid extends lophophore, expands tentacles
Retract lophophore by muscle action:
- lophophore pulled in by retractor muscles
collapses over
- collar folds over withdrawn tentacles
tentacles
compare and contrast
feeding in this group
with sipunculan worms!
Class Gymnolaemata
Order Cheilostomata
- polymorphic zooids
- exoskeleton made of chitin + calcium carbonate
- non-stoloniferous growth:
walls of the zooids are attached
to each other
 colony grows as a continuous
sheet, all zooids fused together
Class Gymnolaemata
Order Cheilostomata
- hard casing causes a problem: how to pressurize coelom?
- solution: flexible frontal membrane on top
- muscles pull membrane down,
pressurizing coelom
lophophore extends
In most successful group,
membrane = the ascus
- internal, for protection;
outer wall is solid
- pore lets seawater in
when ascus is pulled down
Schizoporella unicornis
showing orange opercula
covering zooids
Eurystomella
bilabiata,
only food of the
“Hopkin’s Rose”
sea slug
lophophores extended
Bugula
neritina
- common fouling organism, worldwide
Contains defensive compounds, the bryostatins
- made by a unique bacterial symbiont
- chemicals protect the large, lecithotrophic larvae
from predation during their brief planktonic journey
- in clinical trials as an anti-cancer drug
Bryozoans may be sister to a clade composed of 1 or 2
phyla that was not historically considered “lophophorates”
Bryozoa
Cycliophora
Entoprocta
- based on molecular
analysis of protein
sequences
Polyzoa
Phylum Entoprocta
150 species
- solitary or colonial filter feeders
- feed with anterior ring of ciliated tentacles, but anus opens
inside the ring (ento = within, procta = anus)
- no blood vessels, U-shaped gut
- spiral, determinate embryonic cleavage
(typical protostome kind)
- some species have trochophore-like larvae
embryos + larvae are like other protostomes,
adults are like bryozoans.. close relatives
that develop quite differently
water moves through the ring of ciliated tentacles in the
opposite direction of lophophore flow
bryozoan
water
water
entoproct
Phylum Entoprocta
developing larvae may be found
attached to inside of calyx
family Pedicellinidae
Barentsia benedeni
calyx, with fringe
of tentacles
stalk may have up
to 12 joints on older
individuals
Phylum Cycliophora
~5 species
Close-up of mouthparts of
Norwegian lobster, showing…
Symbion
pandora
Phylum Cycliophora
First reported in 1995
Entire phyla are still
waiting to be discovered
used to stick to
lobster mouth
Phylum Phoronida
2 genera
14 species
- worm-like body inside a chitin tube
- body has a flappy prosome, mesosome w/ lophophore,
and an elongated trunk (metasome)
- U-shaped gut; mouth and anus very close together
- 1 pair of metanephridia, closed circulatory system
- gonads simple, temporary; separate sexes or hermaphrodites
- blastopore becomes mouth (protostome character)
- unique actinotroch larvae
- lophophore is a double row of tentacles
- each tentacle contains blood vessel for
gas exchange, extension of coelom
- food particles brought into ring by current;
then trapped in mucus lining food groove
- gametes proliferate in metacoel of trunk,
released through nephridia, or ruptured out
of tentacle ends
.. similar to many annelid worms; is this
a synapomorphy or a case of
convergent evolution?
Phoronis vancouverensis
Few species = not evolutionarily successful
Can be very ecologically important, however; tubes can form
dense aggregations on local mudflats, creating habitat
Phoronis australis
commensals that attach to the tubes made by cerianthids,
a group of tube-building anemones that live in soft-sediments
Actinotroch larvae
- distinctive flattened head, body ringed with fat tentacles
- ring of cilia at base of body
Phylum Brachiopoda
350 living species
30,000 fossil species
- body enclosed between 2 valves (dorsal + ventral)
- live cemented to bottom, or dig with ventral foot-like pedicle
- valves lined by mantle, creating mantle cavity (as in molluscs)
- U-shaped gut, with or without anus
- 1-2 pairs of metanephridia,
- open circulatory system
- separate sexes; temporary gonads
- blastopore closes;
mouth + anus form secondarily
valves house lophophore
inside mantle cavity
Brachiopod Filter Feeding
ciliary motion
water flow
- Water passes over lateral cilia bands,
which send particles to frontal bands by localized beat reversal
- Frontal cilia then re-direct particles to food groove
Class Inarticulata
Class Articulata
- shells may be equal,
especially in burrowers
- shells usually unequal
- valves not hinged;
attached by muscles
- valves hinged: ventral teeth
lock into dorsal socket
- lophophore w/out skeleton
- lophophore w/ skeleton
- anus present
- no anus
Articulate Brachiopod
- Ventral valve bears teeth that lock into dorsal valve socket
- Adductor muscles close valves; diductors open valves
- contrast w/ bivalve, where springy ligament forces shell
valves open if adductor muscles relax
Brachiopod vs. Bivalve
umbo is dorsal
top valve is dorsal
ventral
ventral
dorsal
ventral
Brachiopod vs. Bivalve
evolutionary loser
350 living spp.
evolutionary winner
7,600 living spp.
Bivalves and brachiopods compete for the same resources;
bivalves have been come dominant, while most brachiopods
went extinct
Key bivalve innovation may have been the mantle fusing into
a siphon for drawing water into the shell