zoo4 honours

ZOO4 HONOURSMark Blaxter 2007-2008 www.nematodes.org

ARTHROPOD ORIGINS AND RELATIONSHIPS

Arthropod origins and relationships

Three main questions:

1. Is Arthropoda a monophyletic group?

2. Which non-arthropod groups are most closely related to Arthropoda?

3. What are the relationships among different arthropod groups?

NB: these questions are inextricably interlinked…

Why do these questions matter?• Inform models of metazoan evolution -

what is the pattern of evolution of morphological and physiological novelty? Are there general evolutionary ‘laws’?

• Arthropods are ~80% of described diversity.


Three main questions:1. Is Arthropoda a monophyletic group?2. Which non-arthropod groups are most

closely related to Arthropoda?3. What are the relationships among

different arthropod groups?

Is Arthropoda Monophyletic?

Monophyly: a natural group that includes ALL the descendents of a particular ancestor

So:

Reptilia is only MONOPHYLETIC if we include Aves

The taxon “marine mammals” is not monophyletic within Mammalia (as it excludes groups that last shared a common ancestor with some non-marine mammals since the last common ancestor of all marine mammals)


According to ‘traditional’ systematic taxonomies,there are four extant classes within Arthropoda

CHELICERATA spiders and alliesMYRIAPODA centipedes and alliesCRUSTACEA crabs and alliesHEXAPODA insects and allies

There is one extinct class

TRILOBITA the trilobites

Trilobites

AncientMarineNo jawsGills on limbs

Chelicerates

Spiders Ticks and Mites Solifuges

Scorpions PseudoscorpionsAmblypygids

Ancient, originally marine, chelicerae, book gills/lungs

Horseshoe crabs

Pycnogonids

Myriapods

Ancientoriginally marineMandiblesTracheae

Crustacea

AncientOriginally marineMandiblesGills on limbs

Hexapoda

YoungTerrestrialMandiblesTracheae

InsectaDipleuraEllipleura



What defines “Arthropoda”?

Bilaterally symmetrical, triploblast, protostomious

Coelomate, but coelom reduced to reproductive and excretory systems

Body cavity is a haemocoel; circulatory system is open




Segmented internally and externally

Teloblastic growth

Tagmosis (minimally cephalon and trunk)Cephalon includes nonsegmental acron and labrum;

Cephalon with lateral faceted eyes and median ocelli

Each segment with appendages

with proximal protopod and distal telopod

Gut complex and regionalised




Segmented internally and externally;

Teloblastic growth

Tagmosis (minimally cephalon and trunk)

Cephalon includes nonsegmental acron and labrum;

Cephalon with lateral faceted eyes and median ocelli

Each segment with appendages

with proximal protopod and distal telopodGut complex and regionalised




Musculature metameric; No circular somatic musculature; Dorsal and ventral longditudinal muscles present

Dorsal CNS ganglia (protocerebrum is ocular, deuterocerebrum antennal)

Paired ventral nerve cords and ganglia




Cilia absent except in some sperm

Growth by moulting (ecdysis) mediated by ecdysone

Cuticular exoskeleton with chitin and resilin/cuticlin, NOT collagen; sometimes calcified




Could these characters have arisen multiple times, independently?

Could the arthropod “grade” have evolved more than once from a common ancestor with the Annelida?

(HOMOPLASY - the convergent evolution of shared characters)

Which non-arthropod groups are most closely related to Arthropoda?

?

(if all arthropods share the same ancestors, they will be monophyletic)


The common ancestor of all Arthropods was probably a ‘lobopod’, similar to extant onychophorans and tardigrades

Onychophorathe velvet worms

TerrestrialSoft-bodiedSegmentedLobopod legsRareViviparousSmallish (cm)

patchy fossil record, but present in Burgess Shale and other faunas (marine)

Tardigradathe water bears

Terrestrial and marineOviparousSoft-bodiedSegmentedLobopod legsCommonTiny (~1 mm or less)

essentially absent from the fossil record


S. Manton and D. Anderson suggested that Arthropoda was polyphyletic

3 independent origins of the arthropod “grade”

HexapodsMyriapods

Onychophorans

Crustacea

Trilobites

Chelicerates

Uniramous limbs

Tracheal system

Biramous limbs

1

2

3These groups also differ in patterns of segmentation in the head

No mandibles


Polyphyletic origin hypotheses have been tested and are less likely than a monophyletic origin

Support for monophyly comes from

Molecular phylogenetic data (that excludes Onychophora and Tardigrada)

Gene arrangements in the mitochondrial genome

Patterns of expression of HOX genes during development

Analysis of limb development and evolution

Close analysis of “tracheal” systems


Panarthropoda

Tardigrada Onychophora Arthropoda


Panarthropoda

TardigradaOnychophora Arthropoda

Do fossils help?

Are there “intermediate” fossils that will help in clarifying the relationships of arthropods and other animals?

Do fossils help?Lagerstätten - fossilifierous sediments with exquisite preservation even of soft-bodied fauna and soft parts of those with shells.see http://palaeo.gly.bris.ac.uk/Palaeofiles/Lagerstatten/

Burgess Shale, Canada 505 MYaSirius Passet, Greenland 518 MYaChengjiang, China 530 MYa

phosphatic sedimentsDoushantuo, China 590-540 MYa

Ediacaran assemblagesEdiacara, Australia 560-540

MYaMistaken Point, NewfoundlandCharnwood Forest, UK

http://palaeo.gly.bris.ac.uk/Palaeofiles/Lagerstatten/








The Burgess Shale location, Jasper National Park, Canada

Burgess Shale animals were killed and covered by the collapse of a marine reef

reconstructions...

Cambrian arthropods from the Burgess Shale

Aysheaia

Chelicerate

Hallucigenia

Trilobite

Crustacean

Onychophorans

Some are ~easily~ slotted into “standard” places in Arthropoda

Cambrian arthropods from the Burgess Shale

Marella

Opabinia

Anomalocaris

Sidneya

...but for others, it is much less easy to shoehorn them into current taxa

Sirius Passet deposits are older, but have some similar taxa

Lagannia, an anomalocarid

...and some unique ones:

Kergymachela

Chienjiang deposits are still above the origin of arthropods

Doushantuo fossils are smallThe animal fossils are EMBRYOS

The Ediacara “fauna” is, at best, enigmatic

Spriggina,a trace fossil, or an arthropod, or an annelid?

Dickinsonia

Tribrachidium

Pteridinium

Do fossils help?

Are there “intermediate” fossils that will help in clarifying the relationships of arthropods and other animals?

Current available fossils post-date the separation of the major animal phyla, or are too enigmatic to really tell us...

... but careful analysis can yield useful information.

end of part one ...


Three main questions:

1. Is Arthropoda a monophyletic group?

2. Which non-arthropod groups are most

closely related to Arthropoda?

3. What are the relationships among

different arthropod groups?

Which non-arthropod groups are most closely related to Panarthropoda?

“lobopod” intermediate

?

ARTICULATA hypothesis: ARTHROPODA plus ANNELIDA


“lobopod” intermediate

Some of the arthropod “defining” characters are SHARED with ANNELIDA (ragworms, earthworms, leeches and allies)

SegmentedAppendages @ one per segmentCNS with ventral cords and segmental gangliaDorsal tubular heart4 or 5 bands of longditudinal musclesOntogeny of segments (teloblastic)

including engrailed expression? Coelomic cavity origins/development

ARTICULATA hypothesis: ARTHROPODA plus ANNELIDA


This hypothesis groups Arthropoda with Annelida and Mollusca

Annelida+Panarthropoda = ARTICULATAArticulata+Mollusca+others = PROTOSTOMIAProtostomia+Deuterostomia= COELOMATA

Coelomata/Pseudocoelomatahypothesis of metazoanrelationships

BUT Arthropods differ from Annelids in important ways

• Annelids do not moult


• Annelids do not moult• Arthropods and Annelids have very different larval stages

Trochophore Nauplius

?


• Annelids do not moult• Arthropods and Annelids have very different larval stages• The arthropod body cavity is a haemocoel, while Annelid body cavities are coelomic compartments

Careful selection of data yielded a very different hypothesis

Initial analyses of single genes yielded phylogenies congruent with Coelomata-Pseudocoelomata

Aguinaldo AMA, Turbeville JM, Linford LS, Rivera MC, Garey JR et al.: Evidence for a clade of nematodes, arthropods and other moulting animals. Nature 1997; 387: 489-493.

Adoutte A, Balavoine G, Lartillot N, Lespinet O, Prud'homme B et al.: The new animal phylogeny: reliability and implications. Proc Natl Acad Sci USA 2000; 97: 4453-4456.


Using all the orthologous genes from

animals that have had their whole genomes

sequenced supports

Nematoda as a sister to (Arthropoda +

Chordata)


...but using data derived

from expressed sequence tags

(“partial genomes”) rejects

Coelomata in favour of

Lophotrochozoa–Ecdysozoa–

DeuterostomiaPhilippe H, Lartillot N, Brinkmann H: Multigene analyses of bilaterian animals corroborate the monophyly of Ecdysozoa, Lophotrochozoa and Protostomia. Mol Biol Evol 2005.

Jones M, Blaxter M: Evolutionary biology: animal roots and shoots. Nature 2005; 434: 1076-1077.

This hypothesis groups Arthropoda with Nematoda

Nematoda+Panarthropoda = ECDYSOZOAAnnelida+Mollusca+... = LOPHOTROCHOZOAEcdysozoa+Lophotrochozoa = PROTOSTOMIA

Ecdysozoa-Lophotrochozoa-Deuterostomiahypothesis of metazoanrelationships

Priapulida

TardigradaOnychophora

KinorhynchaGastrotricha

Loricifera

Nematoda

Nematomorpha


Morphological characters that link the “Ecdysozoa”

• moulting (ecdysone controlled in Arthropoda; mechnisms still unknown, but not simply ecdysone in other taxa)

• lack of cilia (except in neural structures and some sperm)

• triradiate pharynx (Nematoda, Onychophora, Tardigrada, and Pycnogonida within Arthropoda)

Pycnogonum littorale (from South Queensferry)

What are the relationships among different arthropod groups?

The three possible trees for the four extant Subphyla of Arthropods


Each tree can be rooted in one of five places...


Eurypterid

Limulus, horseshoe crab

Chelicerata may be the most ancient arthropod group...

If we believe/suspect/have data to showthat Chelicerata are basal, then we again havea choice of three possible trees...


Hypotheses based on morphology group Hexapoda with Myriapoda in a clade Uniramia


Evidence:• tracheal gas exchange system• uniramous appendages• Malphigian tubules• loss of 2nd antennae• loss of mandibular palps

Hypotheses based on morphology group Hexapoda with Myriapoda in a clade Uniramia. Crustacea have been grouped with the Uniramians as Mandibulata

HexapodaMyriapoda

Onychophoraa

Crustacea

Trilobita

Chelicerata

Mandiblulata

The ‘mandibulate theory’


Hypotheses based on morphology group Hexapoda with Myriapoda in a clade Uniramia. An alternate view places Crustacea closer to Chelicerata: the TCC clade.

HexapodaMyriapoda

Onychophoraa

Crustacea

Trilobita

Chelicerata

The ‘TCC hypothesis’

TCCclade


Sequence analyses and developmental evidence• strongly link Crustacea and Hexapoda• suggest that similarities between

Hexapoda and Myriapoda are the result of convergence


For example, the ommatidia of Hexapoda and Crustacea have a shared tetrapartite crystalline cone, while other Arthropoda have either fused ocelli (Myriapoda) or a very different anatomy (Xiphosura, Chelicerata)

Sequence and developmental evidence• strongly links Crustacea and Hexapoda• suggests that similarities between

Hexapoda and Myriapoda are the result of convergence

Hexapoda

Myriapoda

Onychophora

Crustacea

Chelicerata



There is still disagreement on the relationship of Hexapoda/Crustacea to the other subphyla

Hwang UW, Friedrich M, Tautz D, Park CJ, Kim W: Mitochondrial protein phylogeny joins myriapods with chelicerates. Nature 2001; 413: 154-157.

Giribet G, Edgecombe GD, Wheeler WC: Arthropod phylogeny based on eight molecular loci and morphology. Nature 2001; 413: 157-161.

Analysis of complete mitochondrial genomes suggests that Hexapoda and Crustacea may be “mutually paraphyletic”


Nardi F, Spinsanti G, Boore JL, Carapelli A, Dallai R et al.: Hexapod origins: monophyletic or paraphyletic? Science 2003; 299: 1887-1889.

Indeed, the presence in lagerstätten fossils of many varied “crustaceomorph” animals suggests to some that all extant arthropod groups may be derived from a “protocrustacean” ancestor


Emergence onto land....

Emergence onto land: The Rhynie Chert

pterygote Insecta

Crustacea

Arachnida, ...

end of part two ...

here is a summary:

Arthropod Origins

• There were many early experimentations in arthropod design that may (or may not!) represent early members of extant major groups.

Arthropod Origins

• There were many early experimentations in arthropod design that may (or may not!) represent early members of extant major groups.• In the past, serious arguments were made for multiple independent events of evolution of the arthropod state. eg Manton’s Chelicerates, Crustacea, and Insects/Myriapods.

Arthropod Origins

• There were many early experimentations in arthropod design that may (or may not!) represent early members of extant major groups.• In the past, serious arguments were made for multiple independent events of evolution of the arthropod state. eg Manton’s Chelicerates, Crustacea, and Insects/Myriapods.• However, current developmental evidence and molecular phylogenetic analyses strongly support monophyly.

Arthropod Origins

• There were many early experimentations in arthropod design that may (or may not!) represent early members of extant major groups.• In the past, serious arguments were made for multiple independent events of evolution of the arthropod state. eg Manton’s Chelicerates, Crustacea, and Insects/Myriapods.• However, current developmental evidence and molecular phylogenetic analyses strongly support monophyly.• The ancestor was once thought to be close to annelids (the “Articulata” hypothesis), but ...

Arthropod Origins

• There were many early experimentations in arthropod design that may (or may not!) represent early members of extant major groups.• In the past, serious arguments were made for multiple independent events of evolution of the arthropod state. eg Manton’s Chelicerates, Crustacea, and Insects/Myriapods.• However, current developmental evidence and molecular phylogenetic analyses strongly support monophyly.• The ancestor was once thought to be close to annelids (the “Articulata” hypothesis), but ...• Modern analyses place Arthropoda within the Ecdysozoa, implying that segmentation may have evolved more than once.

Arthropod Origins

• The common ancestor of all Arthropods was probably a ‘lobopod’, similar to extant Onychophora

Arthropod Origins

• The common ancestor of all Arthropods was probably a ‘lobopod’, similar to extant Onychophora• The Chelicerates, Crustaceans, Myriapods and Trilobites all evolved in the sea. The first three groups invaded the land independently.

Arthropod Origins

• The common ancestor of all Arthropods was probably a ‘lobopod’, similar to extant Onychophora• The Chelicerata, Crustacea, Myriapoda and Trilobites all evolved in the sea. The first three groups invaded the land independently.• Hexapoda appear to have evolved from crustacean ancestors, and Collembola may have an independent origin from other Hexapoda

Arthropod Origins

• The common ancestor of all Arthropods was probably a ‘lobopod’, similar to extant Onychophorans• The Chelicerata, Crustacea, Myriapoda and Trilobites all evolved in the sea. The first three groups invaded the land independently.• Hexapoda appear to have evolved from crustacean ancestors, and Collembola may have an independent origin from other Hexapoda• Some of the similarities among these groups are the results of convergent adaptation to terrestrial life, e.g.

• tracheal breathing systems in insects, millipedes and some spiders• malpighian tubule excretory systems in insects and millipedes.• uniramous legs in Myriapoda and Hexapoda• loss of the second antennae in Myriapoda and Hexapoda

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openis arthropoda monophyletic

monophyletic group

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haemocoel circulatory

excretory systemsbody