INCOMPLETE

VERSION

TRABAJO FIN DE GRADO

Alejandro Damián Serrano 4º de CC. Del Mar

Junio, 2013

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Evolution and adaptive radiation of the phylum Ctenophora

Damián-Serrano, A.1

1Facultad de Veterinaria y Ciencias Experimentales, Universidad Católica de Valencia

San Vicente Mártir (UCV).

INDEX:

1. Abstract

2. Introduction

3. Materials & Methods

- Ctenophore specimen sampling

- Phenomic matrix construction

- Molecular dataset

- Phylogenetic analysis

- Trait mapping

- Species studied

4. Results & Discussion

- Trait history reconstruction using parsimony

- Trait associations

- Cladistic topology

- Description of the cladistic units proposed

- Morphological insights

- Evolution

- Adaptive radiation

5. Conclusions

6. References

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1. ABSTRACT

The outstanding diversity and adaptive radiation of ctenophores in the homogeneous

pelagic realm, where niche overlap is high and barriers to genetic exchange are

diffuse, remains a mystery of the Plankton Paradox. This study aims to estimate the

phylogenetic relationships between extant ctenophores, and develop a preliminary

theory on their diversification mechanisms in the ocean.

Features of the natural history and anatomy of different ctenophores were extracted

from the literature, and analyzed from videographic, photographic and fresh biological

samples from ROV and blue-water SCUBA dives. Phylogenetic trees were built using

phenotypic and 18S molecular data. The resulting trees were compared, and ancestral

nodes were reconstructed using maximum parsimony.

Results show that many currently used taxonomic units are not monophyletic or

inconsistent. Some monophyletic clades share similar feeding strategies, determined

by characteristic trophic ecology, functional morphology, and behavior. The ancestor to

all extant ctenophores was a deep sea cydippoid. The phylogenetic tree for

ctenophores is highly unbalanced by terminal adaptive radiations. Morphological

homoplasy correlates with niche similarity. Most of the basal evolution of extant

ctenophores occurred in the deep sea.

In conclusion, morphology and molecular based phylogenies are complementary for

assessing ctenophore evolution. The actual taxonomic classification for the phylum

Ctenophora is inconsistent and should be thoroughly revised. The cladistic units

described here could be used to guide a new classification. Phenotypical divergence

does not correlate with phylogenetic distance. Adaptive radiation occurs through

allopatric speciation in distinct water masses, driven by key adaptations to exploit new

trophic resources.

2. INTRODUCTION

Ctenophores are a unique animal phylum, for the possession of macrocilia and

adhesive colloblasts (Krumbach, 1925). Their extremely fragile body renders their

study and collection in the ocean complex and expensive (Pugh, 1989), especially for

the majority of species which live at great depth (Lindsay & Hunt, 2005). It was not until

the advent of new techniques and technologies such as submersibles, ROVs

(Remotely Operated Vehicles) and blue-water diving (Hamner, 1975), when scientists

had the opportunity to collect and observe these organisms alive in their environment,

instead of being damaged by conventional plankton nets (Haddock, 2004). This

opened up the way to novel studies on integrative biology of the whole phylum. Other

innovations in molecular biology, such as animal 18S gene and mitochondrial DNA

sequence analysis tools, have permitted many phylogenetic relationship trees to be

discovered this century (Avise, 1994). This has provided new insights on evolution and

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diversification of the extant species in multiple animal taxa (Dunn et al., 2008).

Molecular tools for building phylogenetic trees are generally regarded as a more

reliable method than traditional morphology-based phylogenies. This is based on the

much lower probability of homoplasy in genetic sequences, and therefore in the

misinterpretation of traits, associations, and direction of evolution from interpreting

these phylogenies (Givnish and Sytsma, 1997). Due to technological innovations,

actual zoology has been able to study ctenophores from perspectives such as the

ethological and the phylogenetic, which provide us integral and qualitative

comprehension on the autoecology of these animals in their environment (Price et al.,

1988; Haddock, 2004).

Since the recent discovery of the fossil ctenophore genus Eoandromeda (Tang et al..,

2011) and advanced phylogenetic studies of the whole animal kingdom (Dunn et al.,

2008), the most accepted theory about early radiation in ancestral metazoans is the

“Planulozoa hypothesis” (Wallberg et al., 2005), which considers ctenophores as a

sibling group to both Bilateria and Cnidaria. Recent phylogenetic studies on full

genomes and transcriptomes suggest that ctenophores are probably a sister group to

all animals (Dunn et al., 2008), including Porifera and Placozoa - having developed

independently their neurons (which lack some neurotransmitters such as serotonin,

and have different structures (Jager et al., 2011)) and nervous system when they

became predators (Maxmen, 2013). The earliest fossil of a ctenophore comes from the

Ediacaran period, more than 550My ago, and is regarded as a pelagic species (Morris

& Collins, 1996; Xian-Guang et al., 2004). This suggests that ctenophores might have

been evolving separately as planktonic predators in the ocean for hundreds of millions

of years, and thus renders ctenophores one of the most interesting animal groups for

which to develop their first accurate evolutionary model.

Since the last century, significant attention has been given to the feeding ecology of

ctenophores. Ctenophores are voracious predators of zooplankton (Purcell & Decker,

2005), including larvae of commercially important fish and mollusk species, being

capable of swift depletion of fishery stocks (Purcell, 1990). Many neritic species have

blooming reproduction, being able to spawn very fast and reach high population

densities, which cause severely alterations of the trophic ecology and plankton

composition. One of the most terrible examples was the arrival of the invasive

ctenophore Mnemiopsis leidyi in the Black Sea, which seized local fisheries of

Clupeiformes (Shiganova et al., 2001) by clearing the water from eggs and larvae

(Purcell, 1985). The recovery of the ecosystem and the fisheries came with the

invasion of another ctenophore (Beroe ovata) (Finenko et al., 2003), which feeds on

other ctenophores such as M. leidyi (Swanson, 1974). This example shows how

relevant ctenophore biology can be to society and economy. The risks of further

invasions and fishery seizures in other stocks are still real (Purcell, 1991). Growing

concerns of society on increasing abundance and blooms of gelatinous predators are

evident in the media (Arai, 2001; Condon et al., 2012). In order to understand the

mechanisms which nowadays drive the ecology of ctenophore populations in our

oceans, it becomes necessary to understand which factors forced their evolution in the

past and how they did so. Quoting Sir Alister Hardy talking about ctenophores in 1965:

“Their power of destruction is not surprising once we see their method of obtaining

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food” (inspired by the observations of Main in 1928). This sentence condenses the

sense of relevance of this ‘evolutionary ecology’ approach in ctenophore research.

Biodiversity studies are of interest in the context of ecosystem functioning, since

species diversity has functional consequences, and thus, changes in biodiversity can

alter ecosystem processes and change the resilience of ecosystems (Laakman et al.,

2012). Actual diversity of ctenophore species is poorly understood, where the vast

majority of known species are still undescribed (Lindsay & Hunt, 2005; Gibbons et al.,

2005). The main process involved in the creation of species richness and diversity is

adaptive radiation (Schluter, 2000). Many concepts of adaptive radiation involve a shift

in adaptive zone due to the evolutionary origin of a key innovation, a shift in the

selective regime (as the biotic and abiotic environment) or both (Simpson 1953). This

shift may be accompanied by either exceptional species proliferation, phenotypic

evolution, or both (Givnish 1997; Schluter 2000; Glor 2010; Losos & Mahler 2010).

Despite their very low genetic divergence (Podar et al.. 2001), extant species in the

phylum Ctenophora show a great level of morphological diversity (Fig 1). Much of this

variability appears to be directly related to specialization for feeding on prey of different

sizes, behaviors, and abundances (Haddock, 2007). Because they lack stinging cells to

immobilize prey, they must use other means for its capture, most often mucus and

colloblasts (specialized glue-secreting cells). In addition, there are many ways in which

their giant cilia are used for propulsion, conveying food, and biting or engulfing certain

types of prey (Tamm, 1973; Horridge, 1965; Tamm & Tamm, 1991). Even for marine

biologists, understanding these adaptations, however, is difficult if the ctenophores are

not observed under natural conditions. The wide diversity of foraging and feeding

behaviors observed in lobates, cydippids and cestids provides clues for determining

prey selectivity (Greene, 1986), and thus will lead to a better understanding of the ways

in which ctenophores exploit food resources in the open sea (Matsumoto & Harbison,

1993).

The effects of predation on ctenophore populations in the open ocean are often

dispersed and nonspecific (Purcell & Cowan, 1995; Arai, 2005), so it is unlikely for it to

be a driver of their evolution as a whole. Nevertheless, many species have acquired

interesting antipredatory behaviors, such as the lobe flapping escape motion in

Ocyropsis and Bathocyroe (Harbison et al., 1978; Madin & Harbison, 1978b), the

reactions of Mnemiopsis (Kreps et al., 1997; Titelman et al., 2012) or the

bioluminescent secretions in Eurhamphaea and Mertensia (Jonescu, 1908; Haddock &

Case, 1999). A similar case is the infestation with symbionts such as hyperiid

amphipods (Flores & Brusca, 1975; Yip, 1984), which does not significantly influence

the phenology of ctenophores (Harbison et al., 1977; Sorarrain et al., 2001).

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Fig 1. General anatomy of some of the major groups of described ctenophores. (A)

Cydippid ctenophore Pleurobrachia. The extensive gastrovascular canal system is not

shown here completely. (B) Another cydippid, Lampea, with gametes developing in the

meridional canals. (C) Ganeshid ctenophore, Ganesha. (D, E) Beroid ctenophore,

Beroe. (D) Side view. (E) Aboral view. (F) Platyctenid ctenophore, the aberrant-shaped

Lyrocteis, shown here in layered cutaway view exposing various internal structures. (G)

Another platyctenid, Ctenoplana (aboral view). Only one tentacle is shown. (H) The

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platyctenid Coeloplana. (I) Cestid ctenophore, Cestum. (J) Lobate ctenophore

Mnemiopsis, side view. (L) Lobate ctenophore, Deiopea. From Brusca & Brusca,

(2002).

Many different ctenophore groups inhabit the mesopelagic zone (Lindsay & Hunt,

2005). This environment, abiotically, is very homogeneous and stable, so it does not

seem to be able to trigger a fast sympatric diversification, speciation, and specialization

on the monophyletic descendants of a phylum like ctenophores on its own. Many

others inhabit the epipelagic zone (Esterly, 1914), though less stable than the

mesopelagic, it is even more spatially homogeneous (Hayward et al., 1983). It is

assumed that the pelagic realm holds no significant barriers (Wilson & Hessler, 1987).

This makes allopatric biogeographic speciation an infrequent evolutionary mechanism,

with exception of punctual cases of interoceanic speciation (Oklodkov, 2010). Despite

these assumptions, we can find a vast diversity of animal species in the pelagic realm,

which is a feedback phenomenon, creating multiple niches on which organisms can

specialize through interspecific relationships, most frequently of a predator-prey kind

(Greene, 1985). The depth-size-preysize distribution in ctenophores (Fig 2) shows

interesting trends which might become more conspicuous with a broader taxon

sampling.

Fig 2. Categorical distribution of depth and prey size for some of the most common

ctenophore species seen by the ROVs in the Monterey Canyon area. From Haddock

(2004).

Ultrastructural and physiological characteristics are fairly homogeneous within the

phylum (Hernandez-Nicaise, 1991). As a consequence of this, microscopical

techniques are of little use for taxonomic diagnosis or identification of affinities between

species. Together with their low genetic divergence, this supports the hypothesis of a

very recent common ancestor. Behavior has been a forgotten aspect in the study of

zooplankton, as classical methods with nets and formalin preservatives do not give a

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chance to understand their ethology in their habitat. The importance of ethological

assessment in zooplankton has been remarked by Hamner (1985), as behavior has a

profound effect on the ecological processes it is involved in.

Given the often unconvincing fossil record, it is difficult to establish the sequence

through which ctenophore feeding strategies might have evolved. Some

paleontologists suggest that atentaculate Beroe-like species were first to evolve (Morris

& Collins, 1996), but there is molecular evidence (Podar et al.. 2001) that tentacles

were present in the ancestor of extant species (which are the scope of this work),

suggesting that a loss of tentacles in actual atentaculate ctenophores is the derived

condition. The most important principle in taxonomy is that systematic units should be

natural evolutionary units - the practical aspect must be subordinated (De Queiroz,

1997). The actual arrangement of taxa within the phylum Ctenophora establishes

readily recognizable and practical units (e.g. Tentaculata - with tentacles; and Nuda -

without tentacles). Nonetheless, it has been regarded as inconsistent and inaccurate

by many authors (Ospovat, 1985; Harbison, 1985; Podar et al., 2001). The class Nuda

was proven not basal, and the class Tentaculata, as paraphyletic; in the first attempt of

a molecular phylogeny with ctenophores (Podar et al., 2001). Ospovat (1985) proposed

different class-level taxa for ctenophores, based on the structure of the gastrovascular

system, which has been accepted by certain scientific groups (Mills, 1998). This

classification groups the Beroida with the Ganeshida, the Cryptolobiferida, the Lobata,

the Cestida and the Thalasocalycida in the class Cyclocoela (with orally-connected

meridional canals). The complementary class Typhlocoela includes the Cydippida

(including the Haeckelidae) and the Platyctenida.

Haddock, in his paper on comparative feeding modes (2007), divides ctenophores in 4

groups: tentacle net feeders (1), lobe or body expansions feeders (2), engulfing

feeders (3), and feeding specialists (4).

1) Tentacle net feeder ctenophores, such as the well-known Pleurobrachia pileus

(Tamm and Moss, 1985), have a passive predatory strategy, describing semicircular

swims meanwhile extending their tentilla as a net to capture small prey with their

colloblasts. Other genus such as Hormiphora, Mertensia (Mertensidae family),

Bathyctena, Euplokamis or Callinaria developed similar strategies. They feed on small

copepods (Mills, 1995) and, the Mertensidae – which present longer, stickier and more

robust tentacles, prey on even larger crustacean prey, such as decapods and

euphausids.

2) Those which use lobes or body expansions to aid in the capture of small to medium

size prey. Here we could include numerous species from the order Lobata, including

the Ocyropsidae family; the order Thalassocalycida (Madin & Harbison, 1978a), and

the order Cestida.

3) Those which feed by engulfing or biting off pieces of large gelatinous prey, gathering

ctenophores from the order Beroida, known for being predators of other ctenophores,

due to their large mouths and pharynges, together with their specialized macrocilia on

their oral margins.

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4) Feeding specialists include Lampea and Haeckelia, as salp and narcomedusae

devourers respectively; presenting an oral region and predatory strategy similar to

Beroe (order Beroida). It also includes Aulacoctena from the deep Arctic Ocean,

though there is no published evidence of any kind of feeding on any other gelatinous

zooplankton. Dryodora presents a large oral vestibule, which uses for specialist

engulfing of larvaceans.

In addition to these, we could include the sessile forms (mostly platyctenids), which are

also tentacle net feeders, but they dwell attached to surfaces (onto floating surfaces

like Ctenoplana (Willey 1897), or onto benthic structures like Vallicula (Rankin, 1956)).

The main objective of this work is the integration of the natural history with the

molecular phylogeny, to 1) obtain a comprehensive and accurate picture of the

phylogeny; 2) understand the phenotypic traits underlying the clades; 3) provide a

reliable systematic framework for the phylum Ctenophora based on monophyletic

relationships; and 4) develop a preliminary theory on the possible diversification

mechanisms of extant pelagic ctenophores.

The basic framework for the assessment of the questions posed is the phylogenetic

tree. Comparison of functional biological traits with molecular phylogeny results has

been used before in other animal groups. For example siphonophores, which are

gelatinous colonial predators with a similar niche as ctenophores in the ocean, were

studied in a similar way by Dunn et al. (2005), to describe the evolution of functional

specialization of zooids; or deep sea midwater copepods, as studied by Laakman et al.

(2012), to understand the driving forces of speciation in deep water plankton. Similar

phylogeny revision assessments have been performed on other planktonic predators

such as jellyfish (Bayha et al., 2010).

The difficulty of establishing an accurate phylogeny for ctenophores is due to 6 main

limitations:

1. Lack of consistent fossil record, especially within the radiation period of

the extant lineage (Morris & Collins, 1996; Podar et al., 2001).

2. Lack of slow and irreversibly evolving skeletal parts (Xian-Guang et al.,

2004).

3. Lack of extensive physiological, embryological and ontogenetic

knowledge across the phylum (Mackie, 1976).

4. Simplicity and mutational plasticity of morphological traits (Martinelli &

Springs, 2005), which can plausibly and parsimoniously evolve in multiple

gains and losses across the phylum.

5. Limited reliability of molecular phylogenies, a consequence of the diffuse

signal of traditional (i.e. COI) and transcriptomic markers, with very low

bootstrap values (Haddock, pers. comm.). Circular mtDNA is very hard to

amplify for most species (L. Christianson pers. comm.), and therefore we lack

representation across the phylum.

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6. Relatively few known extant representatives of deep sea branching

lineages (possibly due to frequent bottleneck events), and the vast

undersampling of deep sea species (Gibbons et al., 2005), especially outside

the waters bathing deep-sea research institutions (MBARI, JAMSTEC...).

These issues hamper our ability to understand ctenophore evolution and elucidate

relationships between taxa. With these limitations, it seems impossible to determine a

reliable evolutionary model for Ctenophora with our current knowledge and resources.

Despite the complications, there is still a way to approach this complex question:

through selecting (by discarding datasets which yield low bootstrap values) and

stacking cladistic information from independent sources (Baker et al., 1998) it is

possible to get the whole picture. Most morphological traits in ctenophores are

structurally simple and can be misleading, as they can be convergently evolved with

relatively few genetic mutations (Martinelli & Springs, 2005). Thus, the use of a resilient

molecular marker with less chances of homoplasic affinity becomes necessary (Givnish

& Sytsma, 1997).

With the first attempt of a molecular phylogeny for the phylum Ctenophora (Podar et

al., 2001), the order Cydippida was regarded as a polyphyletic taxon, and it was

observed that the Mertensidae, due to its basal position in the rooted tree, may

probably constitute the basal branch of the tree of extant ctenophores. It was

suggested that the phylum Ctenophora has probably gone through a bottleneck event,

where just one species survived a mass extinction and produced the actual

monophyletic diversity. Considering the fossil record, it is accepted that the first

ctenophores from the Paleozoic lacked tentacles (Morris & Collins, 1996), but all

current species (as it can be inferred by the common ‘cydippid-larva’ developmental

stage) descend from a tentacle-bearing side branch (Harbison, 1985).

This study attempts to clarify a little more about the ‘Plankton paradox’ (Hutchinson,

1961), by typifying the ontogeny of diversity within a planktonic group in the oceanic

realm in a comprehensive integrated approach. Phylogenetic relationships inferred with

both molecular and morphological data are known to show a reliable framework of

actual affinities between species (Felsenstein, 1984). Overlapping trees with biological

traits (i.e. vertical and geographic distribution, functional morphology, prey size, prey

type, foraging and feeding behavior) shall (1) allow more complex inferences in the

light of phylogeny and evolution and (2) elucidate the mechanisms of interspecific

competitive avoidance or exclusion, thus highlighting the key drivers of speciation

processes and biodiversity (Glor, 2010) in the rarely explored pelagic ocean.

Even though the main goal of this study is to assess the process of adaptive radiation,

the approach is not to quantify variables such as speciation rate, diversity,

adaptiveness, extent, environmental correlation or chronology. Neither it is to

categorize evolutionary events as ‘adaptive radiation’ or ‘progressive divergence’, as

evolutionary trend variables are continuous, and no consensus exists on what can or

cannot be categorically regarded as ‘adaptive radiation’ (Olson & Arroyo-Santos,

2009). It is focused on qualitatively describing the processes, causes and directions of

the diversification of species, ecological niches, behaviors and body plans.

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The present study sets out the hypothesis that ctenophores have followed a series of

divergent specializations in a short time from a relatively recent ancestor, by means of

specialization on the capture of prey, for which they had to develop anatomical and

behavioral adaptations. It is expected to obtain clades of species which have

developed a particular feeding mode.

3. MATERIALS AND METHODS

This study was performed in the Monterey Bay Aquarium Research Institute (MBARI)

during spring 2013, but most of the datasets and sample collections used are product

of years of work by researchers in the institution. The general method followed in the

planning of this study to fulfill the goals set was inspired on Baum & Larson (1991)

phylogenetic methodology to study character macroevolution.

Ctenophore specimen sampling:

Shallow living specimens were collected by blue-water diving (Hamner et al., 1975),

and deep sea specimens were collected with remotely operated underwater vehicles

(ROV Tiburon, ROV Doc Ricketts, and ROV Ventana), using detritus samplers and

suction samplers (Robison & Reisenbichler, 1991).

The ROV filmed close-up video tracks of most ctenophore species in the Monterey

Canyon midwaters. Photographs were taken of most specimens through ROV video

frame-grabs, and through the binocular microscope camera in the laboratory (for those

specimens collected with the samplers). Tissue was dissected from samples for

molecular analysis, and was stored frozen at −80ºC. Annotated videos and frame-

grabs from the ROV filming footages were retrieved through the VARS (Video

Annotation and Reference System) of MBARI (Schlining & Stout, 2006).

MBARI cruises have been more frequent in the Monterey Bay area, especially in the

canyon system of the continental shelf. Nevertheless, many midwater-oriented cruises

(with midwater ROV exploration and/or Blue Water Diving activities) were performed in

waters off Hawaii, the Gulf of California, and the Gulf of Mexico.

Phenomic matrix construction:

In order to build a matrix which includes most of the known phenotypic traits of both

described and undescribed species of extant ctenophores, the software Lucid Builder

3.0 was chosen for its plasticity and comfortable interface (McConville, 2011).

Morphological, physiological, behavioral and ecological data was gathered from very

diverse sources.

For described species, a thorough bibliographical revision was performed, where hand

drawn plates, original descriptions (Fabricius, 1780; Rang, 1828; Delle Chiaje, 1841;

Chun, 1879, 1880; Dawydoff, 1903; Haeckel, 1904; Moser, 1907, 1909, 1910;

Mortensen, 1932; Komai & Tokioka, 1940; Matsumoto, 1988; Harbison et al., 2001;

Horita et al., 2011 and many others), zoological revisions (Gegenbaur, 1856; Fol, 1869;

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Fewkes, 1882; Mayer, 1912; Bigelow, 1912, 1919; Fedele, 1940; Komai & Tokioka,

1942 and many others) and specific papers studying a particular trait (Freeman &

Reynolds, 1973; Moore, 1924; Haddock & Case, 1995, 1999; Greene et al., 1986;

Haddock et al., 2009; Carré et al, 1989 and many others) were revised to extract

almost every described biological characteristic. Taxonomic keys (Torrey, 1905;

Krumbach, 1925; Kuhl, 1932; Ralph, 1950; Greve, 1975; O’Sullivan, 1986; Wrobel &

Mills, 2003; Oliveira & Migotto, 2006; Oliveira et al., 2007; Mills & Haddock, 2007) were

used to find interesting traits to look for in the undescribed species.

For undescribed species (and to further the datasets for described species), living

specimens and multimedia records from MBARI’s time series were examined. An

extensive collection of photographic material from video frame-grabs and magnified

laboratory photographs of undescribed deep dwelling ctenophore species from MBARI

cruises were examined. Common traits were scored into the matrix, which grew in taxa

and traits as novel species were discovered and new traits were identified.

Autapomorphic traits (those present in only one species) were also included. Vertical

distribution and size data for non-physically sampled undescribed species was

obtained through the VARS annotation search motors.

Integral behavioral characterization of undescribed species was performed by

extensive examination of MBARI’s video archives. VARS Query was used to locate the

video tapes which contained footages of the target species, and careful examination of

ethological traits was performed at MBARI’s videographic laboratory.

Some specimens of described and undescribed species captured during the cruises

were examined in the laboratory, describing morphological and ecological traits.

Moreover, different experiments were performed on these specimens to deduce and

test certain physiological traits, such as the presence of an inter-plate ciliated groove

(ICG) (Tamm, 1982).

A Shell code script (by S.D. Haddock) was used to convert the output CSV file from

Lucid Builder into a Nexus format (universal for phylogenetic analysis softwares).

Mesquite 2.75 (Maddison & Maddison, 2001) was employed to test the phylogenetic

signal of different traits and taxa sets using maximum parsimony (MP) models. It was

also used to prepare the final ‘morphology and ecology’ data partition for the

phylogenetic analysis, by tagging traits with the appropriate parsimony model

(ordered/unordered) and weighting based on statistical scaling (Wiens, 2001).

The list below contains the ecological and morphological traits (Fig 3) studied,

classified in their respective categories and subcategories. It does not show the

different states for each trait. Ordinal traits appear bold.

Ecology

Environment

Depth range

Latitude range

Coastal waters

Attached to substrate

Benthic

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Behavior

Foraging

Orientation

Displacement

Tentacle disposition

Sinusoidal auricle movement

Biting off pieces of gelatinous zooplankton

Engulfing (with stomodaeum) whole gelatinous zooplankton

Tentacle ambusher

Flytrap lobes

Lobes or bell as ball traps

Spin to eat prey

Antipredatory

Escape direction

Flap lobes to escape

Undulate to escape

Coil up

Turn inside-out

Bioluminescence

Glowing secretions

Bioluminescence wavelength (nm)

Vermiform body contractions

Diet

Prey size fraction

Relative prey size (prey/Predator)

Reproduction

Internal fertilization

Asexual reproduction by fission

Dioecy

Gonads in keels

4 gonads at end of substomodaeal meridional canals

Body

Size

Body Color

Green fluorescence

Body Shape (stomodaeal plane)

Body Shape (tentacular plane)

Compression in stomodaeal plane

Compression in tentacular plane

Compression in the oral-aboral axis

Comb rows

Comb Row Extent (subtentacular comb rows)

Comb Row Extent (substomodaeal comb rows)

Substomodaeal comb rows paired with subtentacular comb rows

Red spots along comb rows

Separation of plates in rows

Inter-plate ciliated groove

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Keels (tentacular plane)

Oral keels

Horns

Vestibule

Mouth width

Lobes

Lobe extent (vs stomodaeum)

Location of the base of lobe

Auricles

Marginal furrow

Papillae

Papillae Type

Statolith

Lips

Lip Color

Papillae surrounding the polar plates

Tissues resistant to formalin

Absence of colloblasts

Sticky mucus

Embryonic stomodaeum

Spots along oral-aboral axis between comb rows

Canals

Meridional Canal Colour

Meridional Diverticulae

Meridional Diverticulae anastomose

Meridional Canal Extent (subtentacular)

Meridional Canal Extent (substomodaeal)

Stomadaeum Colour

Stomadaeum Extent

Stomodaeum shape

Paragastric Diverticulae

Infundibular Canal

Tentacular canals

Interradial canals

Perradial canals

Subtentacular meridional canals' lower than substomodaeal meridional canals

aboral end

Adradial canals connect to subtentacular meridional canals

Adradial canals connect to substomodaeal meridional canals

Meridional canals and paragastric canals fuse at Oral Pole

Basic canal system

Adradial canals exit directly from Infundibulum

Tentacles

Tentacles

Tentacle Color

Tentilla

Club-coil tentilla

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Striated muscle in tentilla

Tentilla run down the lobe

Tentilla spacing

Tentilla size

Tentacle exit direction

Space through which tentacles leave Body

Color of tentacle bulbs

Tentacle bulb length

Tentacle bulb shape (tentacular plane)

Location of tentacle bulbs

Autapomorphies

Stripe on tentacular side of substomodaeal comb rows

Warts along stomodaeal side of substomodaeal comb rows

White rim to mouth

Orange spots up to the oral end of meridional canals

Perradial canals extend 90º from infundibulum to meridional canals

Stomodaeal blind pits

Meridional canals slope towards counterpart

Spiraloid nodules at lobe end

Concentrations of oil droplets

Attach and devour salp chains

Tentilla spring-traps

Shooting lobes forward

Keels (stomodaeal plane)

4 independently coilable flaps

Lobes fused in medusoid bell

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Fig 3. Collection of figures illustrating some of the morphological traits included in the

matrix. (A) Statolith. (B) Position of base of the lobe. (C) Lobe morphology. Left:

Simple; Right: Independent half-lobes. (D) Tentacle exit structure. (E) Canal system of

different species. Dark blue: Meridional canals; Light blue: Adradial canals; Dark red:

Perradial canals; Pink: Tentacular canals; Black: Interradial canals; Undescribed

species 31: Infundibular canal. (F) Polar plates surounding papillae. Right: Simple

papillae; Middle: Arboreal papillae. (G) Tentacle direction. (H) Pairing of comb rows. (I)

Tentacle bulb location. (J) Gonads at the end of subtentacular meridional canals. (K)

Meridional canals diverticulae types. (L) Compression of the body. Red: Tentacle

bulbs; Green: Polar plates; Purple: Stomodaeum. (M) Keels. (N) Spots running

between comb rows.

Molecular dataset:

16

Researchers in the ‘Zooplankton and Bioluminescence’ laboratory of MBARI have

carefully amplified, sequenced and assembled a collection of genetic marker

sequences from the ctenophores sampled in the cruises. The sequence used in this

study is nuclear 18S gene partial sequence (Fig 4), between the two conserved

regions.

Fig 4. Secondary structure of the small subunit of the eukaryotic ribosomal RNA (18S).

Adapted from Dunn et al., (2005).

Genomic DNA was isolated from tissue samples of 55 ctenophore species. Tissue

samples were either fresh, preserved in 75 to 95 percent ethanol, or frozen (-80°). The

extraction of high molecular weight genomic DNA was achieved by pulverization of

tissue in the reagent DNAzol, followed by centrifugation and ethanol precipitation

(Chomczynski et al., 1997). The complete sequence for the coding region was

amplified from genomic DNA preparations using eukaryotic-specific primers (Medlin et

al.., 1988) via Qiagen Multiplex PCR (30 cycles: 10s at 94°, 60s at 38° to 48°, and 180s

at 72°, after an initial two minute 94°denaturation). The PCR products were directly

sequenced with a 3100 ABI sequencer to retrieve the FASTA sequences.

17

Outgroup sequences including Saccharomyces cerevisiae, Amphimedon

queenslandica, Ciona intestinalis, Drosophila melanogaster and Homo sapiens (within

others) were retrieved from GenBank using the accession numbers (PRJNA128,

PRJNA39517, PRJNA187185, PRJNA164, PRJNA1431 respectively) to their genome

and then using BLAST algorithms (Tatusova & Madden, 1999) to retrieve homologous

18S sequence.

Phylogenetic analysis

MrBayes (Huelsenbeck & Ronquist, 2001) is the software employed in this study for

the integral heuristic tree inference, using algorithms optimized for each data set.

Therefore, the morphological-ecological dataset was analyzed with MP (Lamboy,

1994), and the 18S molecular dataset was analyzed with maximum likelihood (ML)

Bayesian inference algorithms (Goldman et al., 2000). The program resamples the

datasets using Markov Chain Monte Carlo (MCMC) (Rambaut & Grass, 1997) to obtain

the probability distributions with which to build the tree topology (Nylander et al., 2004).

The model parameters were set as standard, with equal weighting for the molecular

data (Olmstead, 1996). The morphological-ecological matrix had the weights assigned

with Mesquite 2.75 according to statistical scaling (Wiens, 2001) of ordinal variables.

Non-ordinal trait variables were equally weighted.

Trait mapping

Once the phylogeny was inferred from the available data, the morphological,

ethological and ecological traits were traced onto the resulting tree topology using the

tool ‘Trace character history’ in Mesquite 2.75. The phenotypic and ecological

characters for each ancestral branch were retrieved (Schluter et al., 1997; Heath et al.,

2008) and examined comparatively with other branches and with their derived extant

species, as in Pagel (1994).

Correlations between traits were studied using clustering methods in R, freely available

in the package mclust (Fraley & Raftery, 2006) from the CRAN-project libraries. The

clustering criteria were based on the shared taxa bearing such traits (Butterworth et al.,

2005). The program read the morphological data from a binary coded version of the

Mesquite phenotype Nexus matrix (translated using a Shell code script by S.D.

Haddock). This way it was possible to observe which traits evolve together, and what

species they share (Díaz-Uriarte & Garland, 1996).

Species studied

Most of the species examines for this study are undescribed species which lack a Latin

name, but a provisional numeration is given (Fig 6). Some of them have only been

filmed by the ROV camera in situ, and were not collected for closer examination and

molecular analysis. The morphological overview matrix includes species (such as

Ganesha sp., or Lobocrypta sp.) which have only been described once (Dawydoff,

1946), but never seen or reported again (Haddock, comm. pers.). In these cases, only

the morphological data could be retrieved (by examining the bibliographical material),

with scarce ecological data besides distribution. Some described species were not

included in this study because of their doubtful description (some described species

are based on fragmented holotypes or synonymized from juvenile forms) or to avoid

18

phylogenetic redundancy, filling terminal branches with all their species, when they can

be represented with just a few.

19

20

Fig 5. Close-up photographs, in situ photographs and hand drawings of the described

species. Square brackets contain the credit corespondance for the photograph. (A)

Aulacoctena acumiata Mortensen, 1932 [E. Widder]; (B) Bathocyroe fosteri Madin &

Harbison, 1978 [S.D. Haddock]; (C) Bathyctena chuni (Moser, 1909) [S.D. Haddock];

(D) Beroe abyssicola Mortensen, 1927 [MBARI]; (E) Beroe cucumis Fabricius, 1780

[S.D. Haddock]; (F) Beroe forskali Milnedwards, 1841 [S.D. Haddock]; (G) Beroe

gracilis Künne, 1939 [S.D. Haddock]; (H) Beroe ovata Brugière, 1739 [Browne]; (I)

Bolinopsis infundibulum (Müller, 1776) [S.D. Haddock]; (J) Bolinopsis vitrea (Agassiz,

1870) [P. Humann]; (K) Callianira antartica Chun, 1897 [L. Madin]; (L) Callianira bialata

Delle Chiaje, 1841 [J. Bradley]; (M) Cambodjia elegantissima Dawydoff, 1946; (N)

Cestum veneris Lesueur, 1813 [G. Matsumoto]; (O) Charistephane fugiens Chun, 1879

[S.D. Haddock]; (P) Coeloplana sp. Kowalevsky, 1880 [S.S. Forum]; (Q) Ctenoplana

sp. Korotneff, 1886 [G.R. Harbison]; (R) Deiopea kaloktenota Chun, 1879 [S.D.

Haddock]; (S) Dryodora glandiformis (Mertens, 1833) [S.D. Haddock]; (T) Euplokamis

dunlapae Mills, 1987 [S.D. Haddock]; (U) Eurhamphaea vexilligera Gegenbaur, 1856

[S.D. Haddock]; (V) Ganesha annamita Dawydoff, 1946; (W) Haeckelia beehleri

(Mayer, 1912) [S.D. Haddock]; (X) Haeckelia rubra (Kölliker, 1853) [S.D. Haddock]; (Y)

Hormiphora californiensis (Torrey, 1904) [S.D. Haddock]; (Z) Kiyohimea usagi

Matsumoto & Robison, 1992 [G.R. Harbison]; (A’) Lampea pancerina (Chun, 1879)

[S.D. Haddock]; (B’) Lampocteis cruentiventer Harbison et al., 2001 [G. Matsumoto];

(C’) Leucothea pulchra Matsumoto, 1988 [P. Hamner]; (D’) Lobatolampea tetragona

Horita, 2000 [Toba Aquarium]; (E’) Lobocrypta annamita Dawydoff, 1946; (F’)

Mnemiopsis leidyi Agassiz, 1865 [K. Bayha]; (G’) Mertensia ovum (Fabricius, 1780)

[S.D. Haddock]; (H’) Neis cordigera Lesson, 1829 [G.R. Harbison]; (I’) Ocyropsis

maculata (Rang, 1828) [S.D. Haddock]; (J’) Ocyropsis crystallina (Rang, 1828)

[CEBIMAR]; (K’) Pleurobrachia pileus (Müller, 1776) [S.D. Haddock]; (L’) Pleurobrachia

bachei Agassiz, 1860 [S.D. Haddock]; (M’) Thalassocalyce inconstans Madin &

Harbison, 1978 [S.D. Haddock]; (O’) Vallicula multiformis Rankin, 1956 [A. Migotto];

(P’) Velamen parallelum (Fol, 1869) [S.D. Haddock]. Drawings are original from

Dawydoff (1946). Pictures are not to scale.

21

[[ DUE TO THE PRESENCE OF UNPUBLISHED DATA, MATERIAL AND

UNDESCRIBED SPECIES OF WHICH CREDIT CORRESPONDS TO STAFF FROM

THE MONTEREY BAY AQUARIUM RESEARCH INSTITUTE, THE RESULTS OF

THIS SENIOR THESIS MAY NOT BE DISPLAYED IN THIS VERSION ]]

To request a full version please contact:

-Author: alex_ds_8@hotmail.com

Or

-Advisor: haddock@mbari.org

22

5. CONCLUSIONS

Extant ctenophores make up a monophyletic group, which evolved and radiated rapidly

from a relatively recent common ancestor, which would probably resemble some of the

extant deep sea cydippids.

Some monophyletic ctenophore clades share similar feeding strategies, determined by

a set of characteristics including trophic ecology, functional morphology and behavior.

Morphological traits in ctenophores coevolve together to adapt to a particular niche or

trophic specialization.

Cydippoid ctenophore phylogeny is best resolved with molecular data, whilst affinities

within more specialized ctenophores can be well inferred using morphological data.

The phylogenetic tree for ctenophores is highly imbalanced by terminal adaptive

radiations, which suggest a ‘punctuated equilibrium’ phenomenon in their evolutionary

history.

The actual taxonomic classification for the phylum Ctenophora is inconsistent with

every phylogenetic study carried out and should be thoroughly revised.

The cladistic units described here could be used as a guide for a new classification.

Phenotypical differentiation is not correlated with phylogenetic distance in the phylum

Ctenophora.

Adaptive radiation in ctenophores occurs through allopatric speciation in distinct water

masses, where a key adaptation allows new resource exploitation. This leads to

thriving, and secondary phenomic optimization of the speciating population.

Competitive exclusion is avoided by means of specialization on different prey

organisms and depth range.

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