Ecdysozoa III: Myriopoda and Pancrustacea
The remaining arthropod diversity falls into Mandibulata, whose living members include:
- Myriapoda (centipedes, millipedes, and kin)
- Pancrustacea (traditional "crustaceans" plus insects and their kin)
Evolution of the concept:
The phylogenetic hypothesis of Mandibulata reflects phylogenetic work of the last decade by both molecular (E.G. Regier et al. 2010.) and morphological (E.G. Legg et al. 2013.) workers. It differs from the traditional taxonomy that still appears in many texts, where Hexapoda and Myriapoda form Uniramia - the arthropods without biramous appendages. Traditionally, there was no conviction that Uniramia and Crustacea were particularly closely related. Key aspects of the emerging consensus:
- Myriapods, hexapods, and "crustaceans" are found to form a monophyletic Mandibulata (whose monophyly is well supported by molecular, developmental, and morphological analyses. (E.G. Mouthparts are derived from three sets of limbs whose homology are demonstrated by morphological similarity and gene expression.))
- Hexapoda (but not Myriapoda) is found to be nested within Crustacea, rendering traditional Crustacea paraphyletic and sinking Uniramia completely.
Grasshopper mouthparts from Urban Entomology, UC Riverside
- A head with several pairs of specialized mouthpart appendages.
- A trunk that may display homonomous segmentation (Myriopoda) or be divided into:
- Thorax with walking appendages
- Abdomen with swimming appendages or lacking appendages
About mandibulatan head appendages: Whereas the equivalence of head appendages in trilobites and chelicerates is straightforward, those of Mandibulate are complex. We see, from front to back:
- Antennae: The "first antennae" or "antennule" of crustaceans and the only antennae of others.
- Second antennae: In crustaceans only, a second pair of antennae
- Labrum (sing. labra - right): A midline structure that functions as an "upper-lip."
- Mandibles: For shearing, piercing, and processing food.
- Maxillae: Ancestral biramous appendages for manipulating and tasting food. The slender exopodite is called a maxillary palp (in aquatic crustaceans, the mandible also bears a palp.) Ancestrally, first and second maxillae were present.
- Maxillae can be fused or modified into derived structures. In the example of the insect (right) the second maxillae are fused to form a labium that functions like lower lip.
This katydid posed with its mouthparts for me.
Recall that Mandibulata encompasses the living arthropods characterized by mandibles and two pairs of maxillae. This group encompasses over 75% of living animal diversity. With that much diversity, it is a wonder that with the application of phylogenetic techniques and the illumination offered by fossils, we understand its evolutionary history as well as we do. In this presentation we follow the results of Legg et al. 2013.
Living Mandibulate Diversity:Falls into two major groups:
- Diplopoda - millipedes (right)
- Chilopoda - centipedes
Sally lightfoot - Grapsus grapsus
- Hexapoda - Insects and their kin
- A bewildering variety of traditional "crustaceans" (paraphyletic)
- Bradoriida: (Cam. - Early Ord.) Tiny planktonic bivalve arthropods. (Do not confuse with bivalve stem-arthropods or with ostrocods.) Anterior two appendages may be homologs of antannae 1 and 2.
- Marellamorpha: (Cam. - Early Dev.) The classic Burgess Shale fossil Marrella splendens is representative of a group that persists into the early Devonian. It's trunk appendages are plesiomorphic biramous, and unspecialized, but the first two may be homologs of antennae 1 and 2.
- "Orsten taxa:" (Cam.) The analysis of Legg et al. 2013. recovered a paraphyletic group of taxa from the Orsten Konzervatlagerstätte. One interesting surprise is the presence in this group of the tiny bivalve "trilobite" Agnostus. This adds fuel to the discussion of whether agnostids are, after all, trilobites.
- Phosphatocopina (Cam.) Yet another group of planktonic bivalve arthropods. Long considered to be ostracods, they are distinguised by details of limb morphology.
Myriapoda: (Sil. - Rec.)
Mandibulate arthropods with honomous trunks (i.e. with repeating unspecialized mdules). Whether they represent the first fully terrestrial animals depends on the resolution of claims that some early scorpions were actually aquatic. They were major components of the Silurian and Devonian land faunas, achieving large size as predators and as detritivores and grazers.
- Each segment bears paired repugnatorial glands that secrete noxious chemicals.
- Breathing is with a tracheal system
- The second antennae are lost (convergent with Hexapoda.)
- Symphyla: (Neog. - Rec.) Tiny eyeless inhabitants of soil and leaf-litter
- Pauropoda: (Neog. - Rec.) Tiny inhabitants of soil and leaf-litter. Each trunk tergite covers two body segments.
- Diplopoda: (Sil. - Rec.) Millipedes.
- Chilopoda:(Sil. - Rec.) Centipedes.
Narceus americanus from Wikipedia
- First antennae (only!)
- First maxillae united to form a "lower lip" (the gnathochilarium.)
- The following body segment which would bear a second maxilla in most arthropods has no appendages.
- Trace fossils that could be made by myriapods extend to the Ordovician.
- Pneumodesmus newmani (Middle Silurian) is the earliest fossil millipede and the earliest fossil arthropod to show traces of a tracheal system (Wilson and Anderson, 2004.)
- Arthropleuridea: (Sil. - Perm.) Long known as giant myriapods, arthropleurids have recently been shown to belong within Diplopoda. Their heyday was the Carboniferous - the source of their best fossils and trackways. Their fortunes waned during the early Permian along with the coal swamp environment they favored. Characteristics:
- Big - up to 2 m. length
- With specialized lateral lobes on their tergites, and limb specializations.
- Oddly, although known from good fossils, there are no traces of a tracheal system. Could they have been semi-aquatic?
Scutigera coleoptrata from Dirk's Pest Management Specialists
Tagmosis: Centipedes have a single pairs of limbs, spiracles, etc. per body segment (plesiomorphic). Head appendages are plesiomorphic for Myriapoda:
- first maxillae
- second maxillae
Chilopod fossil record:
- Body fossils of centipedes known from the latest Silurian. (See Edgecomb and Giribet, 2007 for a review of centipede evolution.)
Myriapod mystery: Given that Pancrustacea and Arachnomorpha were ancestrally marine, we would expect the earliest myriapods to be marine also, however definite marine myriapods elude us. Budd et al., 2001 report on a possible Upper Cambrian form, Xanthomyria spinosa , from Siberia. Inconclusive, but consistent with watt we might expect.
Pancrustacea:Pancrustacea (equivalent to "Tetraconata" of some authors) contains all traditional crustaceans and hexapods. Work of the last decade has produced the growing consensus that "crustacea" is paraphyetic with respect to Hexapoda, but there is no clear consensus of exactly where, within Pancrustacea, hexapods go. For now, we follow the morphology-based analysis of Legg et al. 2013., but interested students should also review the molecular result of Regier et al., 2010.
Nauplius larva from Vatten-Kikaren
- Development from nauplius larva in which the anterior head appendages form first.
Pancrustacean head comparison from The Snodgrass Tapes
- Second antennae (which are often quite large)
- Mandibular palps
Pancrustacean tagmata from Crustacea - The University of Bristol
- Thorax (often covered with a carapace) with biramous limbs that can be specialized as:
- Maxillipeds: accessory feeding appendages
- pereopods: walking limbs
- Abdomen with:
Major Pancrustacean GroupsBefore discussing pancrustacean phylogeny, an inventory of major monophyletic groups:
- Small: Typically around 2 mm. Largest living species up to 30 mm. Largest fossil on record was 80 mm.
- Lives within an expanded bivalve carapace. This is homologous to the carapace of other crustaceans, but with a mid-line hinge, allowing to to be closed over the rest of the animal.
- The posterior body is greatly reduced.
- Seven pairs of appendages are present, of which the first five are the antennae and mouthparts. These do double-duty as swimming organs.
Until recently, Ostracoda and Thecostraca (the barnacles) would have been united in the clade Maxillopoda however recent analyses do not find this to be so.
- Begins life normally enough, as small crustacean with bivalve carapace. Soon attaches by the head to hard substrate, sheds carapace and secretes a set of distinct calcareous plates that are non-homologous to those of other arthropods.
- Thoracic limbs modified to form suspension-feeding cirri.
- Balanomoprha: Acorn barnacles.
- Lepadomoprha: Goose-neck barnacles. The adult plates are non-homologous with those of balanomorphs (?) and the creature is anchored to the substrate by means of a fleshy peduncle.
Tanymastix stagnalis by JFCART from Flickriver.com
- Small, <10 mm.
- Variable number of thoracic limbs
- Basal section of thoracic limbs developed as paddles that also serve as gills. Hence the name "gill-footed." (Even though the typical exopodite ramus is suppressed.)
Copepopd from Wikipedia
- Tiny, <2 mm.
- Depend on simple diffusion for gas exchange, thus gill and heart are reduced.
- In many, there is a single median eye.
Cephalocarid from Ark in Space
Spelonectes sp. from UC Berkeley Museum of Paleontology
- All post-cephalic appendages derived for swimming.
- Remipedes have morphologically adapted for swimming on their backs.
- Remipede mouthparts are raptorial and seem to be modified for transmitting venom, but we don't really know how they feed.
Silverfish from UC Berkeley Museum of Paleontology
Proper insects and their close relatives.
- Like crustaceans, the insect body is tagmatized into a cephalon, thorax, and abdomen
The current state of the art is unsettled, with large areas of disagreement between molecular and morphological results:
- Molecular: Regier et al., 2010
- Morphological: Legg et al. 2013.. Note, the synopsis of their result above omits many fossil taxa. Interested students should consult the publication.
Points of Agreement:
- Miracrustacea: Remipedia and Hexapoda are closely related. Seems odd, but each group has fossil relatives that, like Hexapoda, have replaced the second antenna with an appendage-free intercalary segment. Of course, this makes traditional "Crustacea" paraphyletic.
- Little guys: Thecostraca, Copepoda, and Branchiopoda are closely related in both results. Legg et al. refer to this as Entomostraca.
Significant Points of Disagreement:
- Ostracoda: Either ostracods are the sister taxon to all other pancrustaceans, or they are nested within Entomostraca with the other little guys.
- Cephalocarida: Members of Miracrustacea or Entomostraca?
- Malacostraca: Are they closer to Miracrustacea or nested among the little guys? The molecular result supports a pleasing dichotomy between pancrustaceans closer to insects and those closer to the major marine groups (Vericrustacea) The morphological result is much more stratigraphically congruent.
Eocarid Anthracaris gracilis from Mazon Creek Fossils
- The common ancestor was probably a shrimp-like creature.
- Eight pairs of thoracic appendages broken down into:
- three pairs of maxillipeds for food manipulation
- five pairs of walking limbs. Note: these remain biramous, even though the gills are typically enclosed by the carapace.
- up to three anterior pairs of walking limbs may bear chelae (lobster pincers are robust examples)
Hoplocarid Odontodactylus scyllarus from Wikipedia
- Phyllocarida: (Cam. - Rec.) Large bivalve carapace. Yet another entry in the bivalve arthropod ecospace.
- "Eocarida" (Dev. - Per.) Shrimp-like crustaceans of Late Paleozoic coal swamps. (E.g. Anthracaris gracilis< above right from Mazon Creek.)
- Hoplocarida: (Right) (Dev. - Rec.) Enlarged raptorial first walking limbs. Living members comprise Stomatopoda. Capable of fastest measured movements by any animal. Large eyes. Fossil record begins in the Devonian (Jenner et al., 1998).
- Syncarida (Carb. - Rec.) Lacking carapace, thus revealing segmented thorax with biramous appendages. Thought to have gone extinct in Permian until living specimens found in Tasmania. (E.g. Acanthotelson stimpsoni from Mazon Creek.)
- Peracarida: Include marine and terrestrial isopods - "pill-bugs."
- Decapoda: (Dev. - Rec.) Include any crustacean you have ever considered eating.
- Body has 20 segments, six for the head, eight for the thorax, and six for the abdomen:
- Occupy many habitats, from deep ocean to fresh water and land (almost)
A rogue's gallery of interesting decapods:
- Brachyura: Crabs - Abdomen reduced and flattened. In adult, it is folded beneath the thorax, offering protection from dessication and facilitating movement.
- Anomura: hermit crabs, among whom the abdomen is modified to accommodate mollusk shells.
- Astacidea: Lobsters, cray-fish - Delicious. M'mmm
- Achelata : Spiny lobsters (M'mmm) and slipper lobsters (AKA Moreton Bay bugs - Ahhhh.)
Bristletail from Flickr
Alas, insect cuticle is not calcified. Thus, their fossil record is poor compared to that of crustaceans (though not as bad as you might think). What there is comes largely from Konzervat-Lagerstätten
Insect head appendages from Scioly.org
- The head bears:
- Compound eyes and ocelli .
- First antennae only.
- Second antennae lost.
- Mandibles (without mandibular palp)
- First maxillae
- Second maxillae fused to form a labium or lower lip .
- the head is set off from the thorax by a flexible joint, unlike in aquatic crustaceans
- The thorax bears:
- three pairs of uniramous walking legs
- The abdomen bears:
- Ventilation is exclusively by means of a tracheal system, in which tracheae take in air through spiracles and deliver it directly to the tissues. The tracheae are lined with cuticle that is shed during ecdysis. Note that by this means, insects are able to achieve aerobic scopes approaching 300 (compare to 10 for mammals) (E.G. Hoverflies mate while hovering. Can YOU do that?).
- The head bears:
Hexapod Phylogeny: (Taken from Tree of Life.)
Basal hexapods are sometimes termed "Parainsecta" and include creatures like:
- Collembola: (Dev. - Rec.) Springtails. Cerci modified for jumping. Includes the earliest fossil hexapod, Rhyniella praecursor.
- Protura: (No record) Tiny (2 mm) eyeless, lacking antennae, with enlarged sensory forelimbs.
- Diplura: (Carb. - Rec.) Eyeless predator.
The basal proper insects form part of a paraphyletic grade group - "Apterygota," wingless insects, including:
Doomed adult mayfly
- Paleodictyoptera: (Carb - Perm) Extinct group of large bodied insects (largest with 50 cm. wingspans.) with three wing pairs and piercing/sucking mouthparts. Possibly paraphyletic.
- Ephemoptera: (Mayflies, Carb. - Rec.) Spend most of life as fresh-water aquatic opportunistic feeders. They breathe using gills derived from abdominal styli (I.e. the plesiomorphic arthropod pattern.) Mayflies metamorphose into winged adults for a brief life of mating. As adults (right), living members have no functional mouthparts. This is apomorphic. Indeed, Permian fossil mayflies appear to have had proper mouthparts (Prokop and Nei, 2011).
- Odonata: (Dragonflies and damselflies. Perm.-Rec.): Extremely skillful fliers and aerial predators. Spend their youth as aquatic predators (using specialized protrusible labium to snare prey), then metamorphose into winged adults. Unlike mayflies, they spend months as adults feeding and mating. Some odd things: It is tempting to assume that odonatans ancestrally had life cycles like mayflies, and yet:
- Although fossil adult odonatans were around in the Pennsylvanian, we find no fossils of their aquatic nymphs until the Jurassic. (Indeed, fossils of crown-group Odonata occur only back to the Jurassic. Stem-group odonatans occur as early as the Carboniferous)
- The most phylogenetically basal odonatans, the Petaluridae, lay eggs and spend their youth in moist soil and leaf litter, not in bodies of water.
- Different structures perform the function of gills in different odonatan groups.
Note: before considering the last pterygote group, consider what the life cycle of these "primitive pterygotes" tells us: Unlike apterygotes, pterygotes undergo a partial metamorphosis from and aquatic nymph to a terrestrial imago (adult).
- Evolved a hinged articulation by which the wings could be folded over the back. An obvious advantage if, (unlike dragonflies) you planned to spend time on the ground. This made possible a striking radiation of flying/walking insects. The real breakthrough came when Coleoptera (beetles) transformed their forewings into elytrae (wing covers) to protect the hindwings while on the ground. This made possible behaviors like burrowing and the invasion of microhabitats that might otherwise damage wings. Thus, beetles make up roughly 50% of animal diversity.
- While all arthropods experience discrete instars (growth stages separated by episodes of ecdysis), many Neopterans are holometabolous undergoing a complete metamorphosis between totally dissimilar life stages:
Strudiella devonica from Nature - Garrouste et al., 2012
- The earliest known hexapod is Rhyniella praecursor, a collembolan (springtail) from the Early Devonian Rhynie Chert Konzervat-Lagerstätte.
- Winged insects appear abundantly in the Late Carboniferous. The interval from the Middle Devonian through the Early Carboniferous is called the hexapod gap, in which hexapod fossils are unknown. This, interestingly, encompasses Romer's gap, an analogous gap in the land vertebrate record in the Early Carboniferous. (More on this later.)
- But wait! Garrouste et al., 2012 have just published on Strudiella devonica (right) from the latest Devonian, smack in the middle of the hexapod gap. Although wingless, its jaws resemble those of winged insects. Is it an adult or the nymph of a winged form?
- What allowed Carboniferous - Permian land arthropods to get bigger than later ones? (E.G. dragonflies like Meganeura with 75 cm wingspans, arthropleurid millipedes.) (E.G. Absence of flying vertebrates? Higher [O2]?) Arthropleurids seem to have tracked[O2] faithfully, vanishing in the early Permian. Paleodictyopteroids and protodonatans were out by the Early Triassic. Remaining odonatans had been reduced to current size range. Did the rise of flying vertebrates play any role?
- What selective pressure facilitated the origin of flight? (Exaptation of gills or thermoregulatory structure? Exaptation of structure for surface tension locomotion?)
Insect brain from Bioteaching.com.
The Arthropod Head Problem and the Power of Paleontology:Questions about the homologies of various arthropod head appendages have vexed generations of zoologists. Today, they are finally yielding to the application of developmental, genomic, and paleontological data. First a review. The arthropod brain forms from the integration of the front three pairs of ganglia. Our first tool in homology assessment is which cerebral ganglion an appendage is innervated from. Terminology:
- Protocerebrum the first ganglion pair
- Deuterocerebrum the second
- Tritocerebrum the third
- Protocerebral: The eyes
- Deuterocerebral: The antennae (in mandibulates) and/or chelicerae (in chelicerates)
- Tritocerebral: The remaining mouth parts (in mandibulates) and/or pedipalps (in chelicerates), and the second antennae of crustaceans
- The first antennae of just about all arthropods are homologous to the chelicerae of chelicerates
- The large second antennae of crustaceans occupy a head segment from which appendages have been lost in other arthropods. Link to helpful review and diagram (on right).
Alalcomenaeus sp. from Tanaka et al., 2013
- "Great appendages" of the "megacheiran" Alalcomenaeus are deuterocerebral and likely homologs to antennae and chelicerae (Tanaka et al., 2013).
- The antennae of Fuxianhuia are similarly deuterocerebral (Ma et al., 2012). (See diagram.)
Do all panarthropods fit this pattern? No. Remember the antennae of onychophorans? These have protocerebral innervation. That is:
- they are innervated by the part of the brain that, in euarthropods, is dedicated to the eyes and has no associated appendages
- They are not homologous to the antennae of euarthropods.
Now, from the magic hat of Chengjiang, emerges the radiodont Lyrarapax unguispinus (Cong et al. 2014).
It, too, preserves traces of nervous tissue showing that its raptorial appendages are also protocerebral, and are likely homologs to the antennae of onychophorans.
By Tristan Gardner from Flickr
- All euarthropods except pycnogonids have it.
- It might be a midline structure but embryologically it develops from paired primordia.
- It might be tritcerebral, but developmentally the part of the brain that innervates forms in the front of the brain then migrates backward.
Without the fossils, we couldn't have known.
- Graham E. Budd, Anette E. S. Högström, and Ivan Gogin. 2001. A myriapod-like arthropod from the Upper Cambrian of East Siberia. Paläontologische Zeitschrift, 75(1): 37-41.
- Peiyun Cong, Xiaoya Ma, Xianguang Hou, Gregory D. Edgecombe, and Nicholas J. Strausfeld. 2014. Brain structure resolves the segmental affinity of anomalocaridid appendages. Nature 513, 538-542.
- Gregory D. Edgecombe and Gonzalo Giribet. 2007. Evolutionary Biology of Centipedes (Myriapoda: Chilopoda). Annual Review of Entomology 2007, 52:151-70.
- Romain Garrouste, Gael Clement, Patricia Nel, Michael S. Engel, Philippe Grandcolas, Cyrille D'Haese, Linda Lagebro, ulien Denayer, Pierre Gueriau, Patrick Lafaite, Sebastien Olive, Cyrille Prestianni, and Andre Nel. 2012. A complete insect from the Late Devonian period. Nature 488, 82-85.
- Ronald A. Jenner , Cees H.J. Hof , Frederick R. Schram. 1998. Palaeo- and archaeostomatopods (Hoplocarida: Crustacea) from the Bear Gulch Limestone, Mississippian (Namurian), of central Montana. Contributions to Zoology 67(3): 155-186.
- David A. Legg, Mark D. Sutton & Gregory D. Edgecombe. 2013. Arthropod fossil data increase congruence of morphological and molecular phylogenies. Nature Communications 4(2485).
- Xiaoya Ma, Xianguang Hou, Gregory D. Edgecombe, and Nicholas J. Strausfeld. 2012. Complex brain and optic lobes in an early Cambrian arthropod. Nature 490, 258-261.
- Marco T. Neiber, Tamara R. Hartke, Torben Stemme, Alexandra Bergmann, Jes Rust, Thomas M. Iliffe, Stefan Koenemann. 2013. Global Biodiversity and Phylogenetic Evaluation of Remipedia (Crustacea). PLOS|One May, 2011.
- Jakub Prokop and Andre Nel. 2011. New Middle Permian palaeopteran insects from Lod¸ve Basin in southern France (Ephemeroptera, Diaphanopterodea, Megasecoptera). Zookeys (130): 41Š55..
- Jerome C. Regier, Jeffrey W. Shultz, Andreas Zwick, April Hussey, Bernard Ball, Regina Wetzer, Joel W. Martin, and Clifford W. Cunningham. 2010. Arthropod relationships revealed by phylogenomic analysis of nuclear protein-coding sequences. Nature 463, 1079-1083.
- William A. Shear and Gregory D. Edgecombe. 2010. The geological record and phylogeny of the Myriapoda. Arthropod Structure & Development 39(2-3): 174-190.
- Gengo Tanaka, Xianguang Hou, Xiaoya Ma, Gregory D. Edgecombe, and Nicholas J. Strausfeld. 2013. Chelicerate neural ground pattern in a Cambrian great appendage arthropod. Nature 502, 364-367.
- Dieter Walossek. 1993. The Upper Cambrian Rehbachiella, its larval development, morphology and significance for the phylogeny of Branchiopoda and Crustacea. Developments in Hydrobiology 103: 1-13.
- Heather M. Wilson and Lyall I. Anderson. 2004. Morphology and taxonomy of Paleozoic millipeses (Diplopoda: Chilognatha: Archipolypoda) from Scotland. Journal of Paleontology 78(1): 169-184.