ARTHROPOD ORIGINS AND RELATIONSHIPS Mark Blaxter 2007 2008

ARTHROPOD ORIGINS AND RELATIONSHIPS Mark Blaxter 2007 -2008 ZOO 4 HONOURS www. nematodes. org

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…

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? 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.

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)

Is Arthropoda Monophyletic? According to ‘traditional’ systematic taxonomies, there are four extant classes within Arthropoda CHELICERATA MYRIAPODA CRUSTACEA HEXAPODA spiders and allies centipedes and allies crabs and allies insects and allies There is one extinct class TRILOBITA the trilobites

Trilobites Ancient Marine No jaws Gills on limbs

Chelicerates Spiders Ticks and Mites Scorpions Pseudoscorpions Solifuges Amblypygids Ancient, originally marine, chelicerae, book gills/lungs Pycnogonids Horseshoe crabs

Myriapods Ancient originally marine Mandibles Tracheae

Crustacea Ancient Originally marine Mandibles Gills on limbs

Hexapoda Insecta Dipleura Ellipleura Young Terrestrial Mandibles Tracheae

Is Arthropoda Monophyletic? Monophyly: a natural group that includes ALL the descendents of a particular ancestor 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

Is Arthropoda Monophyletic? Monophyly: a natural group that includes ALL the descendents of a particular ancestor What defines “Arthropoda”? 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

Is Arthropoda Monophyletic? Monophyly: a natural group that includes ALL the descendents of a particular ancestor What defines “Arthropoda”? 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

Is Arthropoda Monophyletic? Monophyly: a natural group that includes ALL the descendents of a particular ancestor What defines “Arthropoda”? 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

Is Arthropoda Monophyletic? Monophyly: a natural group that includes ALL the descendents of a particular ancestor What defines “Arthropoda”? Cilia absent except in some sperm Growth by moulting (ecdysis) mediated by ecdysone Cuticular exoskeleton with chitin and resilin/cuticlin, NOT collagen; sometimes calcified

Is Arthropoda Monophyletic? Monophyly: a natural group that includes ALL the descendents of a particular ancestor What defines “Arthropoda”? 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) ?

Which non-arthropod groups are most closely related to Arthropoda? The common ancestor of all Arthropods was probably a ‘lobopod’, similar to extant onychophorans and tardigrades

Onychophora the velvet worms Terrestrial Soft-bodied Segmented Lobopod legs Rare Viviparous Smallish (cm) patchy fossil record, but present in Burgess Shale and other faunas (marine)

Tardigrada the water bears Terrestrial and marine Oviparous Soft-bodied Segmented Lobopod legs Common Tiny (~1 mm or less) essentially absent from the fossil record

Is Arthropoda Monophyletic? S. Manton and D. Anderson suggested that Arthropoda was polyphyletic Tracheal system Uniramous limbs 1 Hexapods Myriapods Onychophorans Biramous limbs 2 No mandibles 3 Crustacea Trilobites Chelicerates These groups also differ in patterns of segmentation in the head 3 independent origins of the arthropod “grade”

Is Arthropoda Monophyletic? 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

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

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

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 Sirius Passet, Greenland Chengjiang, China phosphatic sediments Doushantuo, China Ediacaran assemblages Ediacara, Australia Mistaken Point, Newfoundland Charnwood Forest, UK 505 MYa 518 MYa 530 MYa 590 -540 MYa 560 -540 MYa

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 Chelicerate Some are ~easily~ slotted into “standard” places in Arthropoda Crustacean Trilobite Aysheaia Hallucigenia Onychophorans

Cambrian arthropods from the Burgess Shale. . . but for others, it is much less easy to shoehorn them into current taxa Marella Opabinia Anomalocaris Sidneya

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 small The animal fossils are EMBRYOS

The Ediacara “fauna” is, at best, enigmatic Spriggina, a trace fossil, or an arthropod, or an annelid? Pteridinium Dickinsonia Tribrachidium

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. . .

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?

Which non-arthropod groups are most closely related to Panarthropoda? ? “lobopod” intermediate

Which non-arthropod groups are most closely related to Panarthropoda? ARTICULATA hypothesis: ARTHROPODA plus ANNELIDA “lobopod” intermediate

Which non-arthropod groups are most closely related to Panarthropoda? Some of the arthropod “defining” characters are SHARED with ANNELIDA (ragworms, earthworms, leeches and allies) Segmented Appendages @ one per segment CNS with ventral cords and segmental ganglia Dorsal tubular heart 4 or 5 bands of longditudinal muscles Ontogeny of segments (teloblastic) including engrailed expression ? Coelomic cavity origins/development ARTICULATA hypothesis: ARTHROPODA plus ANNELIDA

Coelomata/Pseudocoelomata hypothesis of metazoan relationships This hypothesis groups Arthropoda with Annelida and Mollusca Annelida+Panarthropoda = ARTICULATA Articulata+Mollusca+others = PROTOSTOMIA Protostomia+Deuterostomia= COELOMATA

BUT Arthropods differ from Annelids in important ways • Annelids do not moult

BUT Arthropods differ from Annelids in important ways • Annelids do not moult • Arthropods and Annelids have very different larval stages ? Trochophore Nauplius

BUT Arthropods differ from Annelids in important ways • 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

Initial analyses of single genes yielded phylogenies congruent with Coelomata. Pseudocoelomata Careful selection of data yielded a very different hypothesis 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.

Which non-arthropod groups are most closely related to Panarthropoda? Using all the orthologous genes from animals that have had their whole genomes sequenced supports Nematoda as a sister to (Arthropoda + Chordata)

Which non-arthropod groups are most closely related to Panarthropoda? . . . but using data derived from expressed sequence tags (“partial genomes”) rejects Coelomata in favour of Lophotrochozoa– Ecdysozoa– Deuterostomia Philippe 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.

Ecdysozoa-Lophotrochozoa. Deuterostomia hypothesis of metazoan relationships This hypothesis groups Arthropoda with Nematoda+Panarthropoda = ECDYSOZOA Annelida+Mollusca+. . . = LOPHOTROCHOZOA Ecdysozoa+Lophotrochozoa = PROTOSTOMIA

Onychophora Tardigrada Loricifera Nematoda Gastrotricha Kinorhyncha Priapulida Nematomorpha

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

What are the relationships among different arthropod groups? The three possible trees for the four extant Subphyla of Arthropods

What are the relationships among different arthropod groups? Each tree can be rooted in one of five places. . .

Chelicerata may be the most ancient arthropod group. . . Eurypterid Limulus, horseshoe crab

What are the relationships among different arthropod groups? If we believe/suspect/have data to show that Chelicerata are basal, then we again have a choice of three possible trees. . .

What are the relationships among different arthropod groups? Hypotheses based on morphology group Hexapoda with Myriapoda in a clade Uniramia Evidence: • tracheal gas exchange system • uniramous appendages • Malphigian tubules • loss of 2 nd antennae • loss of mandibular palps

What are the relationships among different arthropod groups? Hypotheses based on morphology group Hexapoda with Myriapoda in a clade Uniramia. Crustacea have been grouped with the Uniramians as Mandibulata Mandiblulata Hexapoda Myriapoda Crustacea Chelicerata Trilobita Onychophoraa The ‘mandibulate theory’

What are the relationships among different arthropod groups? Hypotheses based on morphology group Hexapoda with Myriapoda in a clade Uniramia. An alternate view places Crustacea closer to Chelicerata: the TCC clade. Hexapoda Myriapoda Crustacea Chelicerata Trilobita Onychophoraa The ‘TCC hypothesis’ TCC clade

What are the relationships among different arthropod groups? 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)

What are the relationships among different arthropod groups? Sequence and developmental evidence • strongly links Crustacea and Hexapoda • suggests that similarities between Hexapoda and Myriapoda are the result of convergence Hexapoda Crustacea Myriapoda Chelicerata Onychophora

What are the relationships among different arthropod groups? Giribet G, Edgecombe GD, Wheeler WC: Arthropod phylogeny based on eight molecular loci and morphology. Nature 2001; 413: 157 -161. Hwang UW, Friedrich M, Tautz D, Park CJ, Kim W: Mitochondrial protein phylogeny joins myriapods with chelicerates. Nature 2001; 413: 154 -157. There is still disagreement on the relationship of Hexapoda/Crustacea to the other subphyla

What are the relationships among different arthropod groups? 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: 18871889.

What are the relationships among different arthropod groups? 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 Arachnida, . . . Crustacea pterygote Insecta

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