Modifications of the developmental plan fall into two general categories in the evolution of development: heterotopies and heterochronies. Define these two categories and provide an example of each that was discovered in studies of the Australian sea urchins of the genus Heliocidaris .

A. Conserved In Heliocidaris erythrogramma (big eggs) Lost or Modified A mosaic of conserved and radically changed developmental features A. Conserved General rules of A-V axial formation and cleavage (except micromeres) Embryonic cell division rates and time of gastrulation Wnt8 patterning (of the entomesoderm, the A/V axis of the larva and in the hydrocoel-vestibule complex; Wnt genes code for proteins that are integrally involved in animal development) Lost or Modified Cell lines and cell fates (heterotopies) Expression of genes that control the appearance of pluteus features including arms, oral ectoderm and gut (no longer provided by sperm) Wnt expression is accelerated in rudiment both in absolute time as well as relative to the formation of other larval structures. This “heterochrony” have a highly conserved developmental outcome (i.e. development of juvenile sped up ) Ferkowicz and Raff 2001 Kaufman and Raff 2003

Deuterostomes Continued

Phylum Hemichordata (85 species) Class Pterobranchia (sea Angels) Class Enteropneusta (acorn worms) Acorn worms and sea angels Small group of marine worms that show similarities to Echinoderms and Chordates

Tornaria of Acorn Worms Auricularia of Sea Cucumbers Tornaria of Acorn Worms Has deuterostome embryology and resembles in ciliation, feeding mechanism (opposed band) and general appearance an auricularia larva of sea cucumbers Also Adult axial complex similarity (hemal –excretory system) Adult Tripartite coelom (in echinoderms; body coelom, water vascular system and perihemal system which seems to be circulatory in nature)

Adult Characteristics of Acorn Worms 3 partite coelom like echinoderms Proboscis for digging (protocoel) Stomochord first considered a notochord Collar with mouth (mesocoel) Main body is the trunk (metacoel) Up to 100 pair of pharyngeal slits N.S. An epidermal net…. Like the echinoderm nervous system but.. in some a dorsal hollow nerve cord and some with ventral and DNC

Figure 21_01

C H E C E H C H E Conflicting views of Deuterostome phylogeny From Bromham and Degnan, 1999 Traditional Hemi + echino Calcichordate C H E C E H C H E Pharynx DNC larvae Axial complex Fossil stylophoran Proto”D” Proto”D” Proto”D”

(Calcichordate) C E H Conflicting views of Deuterostome phylogeny From Bromham and Degnan, 1999 Fossil Stylophoran (Calcichordate) C E H Proto”D” Hemichordate Echinoderms

C H E C E H C H E Conflicting views of Deuterostome phylogeny From Bromham and Degnan, 1999 Traditional Hemi + echino Calcichordate C H E C E H C H E Pharynx DNC larvae Axial complex Fossil stylophoran Proto”D” Proto”D” Proto”D” -- Mitochondrial and 18s r-RNA sequence analysis strongly supports the Hemichordate-echinoderm (Ambulacraria) relationship to the exclusion of the chordate clade.

C H E How is this possible?? Conflicting views of Deuterostome phylogeny From Bromham and Degnan, 1999 Hemi + echino (Ambulacraria) -- Hemichordates, Fossil Stylophorans, and Chordates all have pharyngeal slits and a dorasal nerve chord, but Echinoderms do not, yet Hemichordates are the sister group of Echinoderms and not of Chordates, and Stylophorans are more related to echinoderms then they are to chordates. C H E larvae Axial complex Proto”D” How is this possible??

Phylum Chordata (49,400 species) SubPhylum Vertebrata (48 K species) SubPhylum Urochordata SubPhylum Cephalochordata Chordate characters are: dorsal hollow nerve cord notochord pharyngeal slits post anal tail Chordates are 1 of 4 deuterostome groups 1400 species of invertebrate chordates

Salps are part of the SubPh Urochordata Video taken in the Tasman Sea https://www.youtube.com/watch?v=5EQGA_4BZ5s

SubPhylum Urochordata Ascidians: sessile filter feeders bag like body covered by a tunic (tunicin is a type of cellulose) solitary Colonial Siphons in out Compound

Endostyle siphon Atrial cavity Pharyngeal slits Ascidians: sessile filter feeders (sea squirts) bag-like body covered by a tunic made of cellulose in some spp. Endostyle (thyroid gland homologue produces iodine rich mucus) siphon Atrial cavity Pharyngeal slits Water enters incurrent siphon passes through porous mucus and exits into atrial cavity through pharyngeal slits. Particles trapped in mucus are swallowed.

a c b Many Ascidians are solitary, but most are colonial (b) or compound (c,d), the latter living within a single tunic sheath an often have a shared atrial siphon. d

Colonial and Compound Ascidians

Megalodicopia hians (Megabyte sea squirt) Deep sea tunicate with a pharynx that is lacking ciliated stigmata

Tasmanian devil-squirt catches prey using a “fly-trap” system

Chordate-like characters of Ascidians are more prominent in the tadpole larva Post anal Tail pharynx Nerve cord Adhesive paillae Notochord endostyle Stomach and intestine

Radical metamorphosis: -- Involves loss of notochord, tail, dorsal hollow nerve cord, swimming musculature -- Rapid growth of region around buccal siphon causes the body to rotate bout 90 deg --Atrium expands --# gill slits increases Atrial siphon Buccal siphon

Tadpole larva shows all key chordate characters: Sea squirts

Sub Phylum Urochordata Class Larvacea: Small (5-6 mm) planktonic, tadpole-like; lives in midwater and secretes a gelatinous house. http://vimeo.com/32278043

Larvacean Tadpole One Hypothesis states that Larvaceans evolved from ascidian tadpoles by a process known as paedomorphosis (a type of heterochrony) but there is new evidence on this relationship (later) Larvacean Tadpole paedomorphosis is the retention by adults of traits previously seen only in the young, and is a subject studied in the field of developmental biology. Neoteny is found in modern humans. Paedomorphism can also be the retention of larval traits which is commonly studied in salamanders. Could happen by speeding up of sexual development (germ line develops faster) and that is called progenesis. Neoteny, the physiological or somatic growth of an organism is slowed down Paedomorphosis: retention by adults of traits previously seen only in the young.

SubPhylum Cephalochordata (lancelets; 2 dozen spp) -- resemble urochordates in feeding biology -- but have much in common with vertebrates: distinct notochord that persists through life dorsal hollow nerve chord that extends to the head, post anal tail…. Post anal tail Digestive system Oral tentacles anus pharyngeal slits Notochord dorsal nerve cord

Dorsal hollow nerve cord Notochord Muscles Gill slit Endostyle Reproductive organ Transverse muscle

SubPhylum Cephalochordata -- feeding biology resembles urochordates -- but have much in common with vertebrates: distinct notochord that persists through life dorsal hollow nerve chord Clearly not a Vertebrate, which have: -- a nerve chord elaborated into a brain -- a protective cranium -- a notochord replaced by a vertebral column But generally accepted as the closest living relative of vertebrates and much studied as a model of vertebrate ancestors

Deuterostome Phylogeny 4 phyla, different from all others but also considerably different from each other Echinoderms, Hemichordates, Xenoturbella, Chordates key characters are embryological, morphological, and more recently genetic A variety of scenarios; as early as 1890 Key questions: echinoderm-hemichordates-xenoturbellids already discussed chordate relationships (Urochordates?)?? ancestral chordate???

How did vertebrate innovations evolve?

Summary : According to Garstang how chordates and vertebrates evolved 1. Chordates formed as a deuterostome larva in an ascidian when its larva was modified to a tadpole-like larva with a notocord, DNC, Endostyle (de novo origin) Tadpole like larva becomes adult Larvacean-like chordate through paedamorphosis (juvenalization) neoteny: morphogenesis is delayed relative to reproductive maturity progenesis: reproductive maturity is accelerated relative to adult morph. Are types of paedamorphosis where adult acquires larval characters 3. Selection favors traits that continue to improve locomotion and activity: complex sensory organs, brain complex musculature, respiration addition of bone ....Vertebrate condition

Garstang speculated that at some point larvae developed gonads and reproduced in the larval stage and a new group of free swimming animals evolved Garstang called this process neoteny (somatic development is slowed), a type of paedomorphosis (adult assumes traits previously seen in juveniles) in which juvenile or larval traits appear in the adult body

Cladogram consistent with Garstang’s view Figure 23_05 Cladogram consistent with Garstang’s view Neoteny here to produce larvacea Selection for increased swimming etc. Neoteny (paedomorphosis) Ascidacea (with tadpole that has evolved chordate characters) In Garstang’s scenario neoteny occurred twice, first to form vertebrate line, later to form larvaceans

Dorsoventral Inversion in Adult: Current Hypothesis that is contradictory to Garstang’s hypotheses explaining origin of chordate characters in a deuterostome larva A dorsoventral inversion of body plan axis in an adult worm like animal was a key event in the evolution of deuterostome characters

Dpp (suppresses neural fate) and its homologue BMP-4 are expressed in a pattern that supports inversion. SOG and its homologues (Chordin) suppress dpp action -Are Hemichordates like acorn worms representative of the common ancestor? -There is new developmental genetic evidence that an axochord in annelids with homologous gene patterning to the notochord ; may have been present in other non chordate invertebrates and could be the precursor of the notochord http://www.mun.ca/biology/desmid/brian/BIOL3530/DB_Ch15/fig15_11.jpg

Cladogram Showing New “Molecular” View Cameron, C.B., Garey, J.R. and Swalla, B. J. (2000)  Evolution of the chordate body plan: New insights from phylogenetic analyses of deuterostome phyla. Proc. Natl. Acad. Sci.97: 4469-4474.   See also Fig. 22-10 Two major clades , Echinoderm-Hermichordates and Chordates Common ancestors of chordate/ hemi-echinoderms had pharyngeal slits, dorsal hollow nerve cord. Larvacean or worm-like animal is ancestor of all chordates?

Cladogram consistent Cladogram consistent with Garstang’s view Figure 23_05 Cladogram consistent with Garstang’s view Cladogram consistent With Cameron’s view

Key New Contributions of Molecular Studies 1. Echinoderm-Hemichordates are sister groups therefore stem deuterostome: adult with pharyngeal slits and dorsal nerve cord 2. Non-Larvacean Urochordates are united in a single derived clade. Larvacean clade is the stem sister group. Larvaceans have no larval stage. So larva played no prominent role in evolution of chordate characters?? 3. New phylogeny contradicts Garstang’s hypothesis in several ways but is neutral yet consistent with respect to D-V inversion and the homology of the annelid axochord and the notochord because the notochord might have originated in a pre-larvacean-like worm.

A consensus cladogram of deuterostome groups based on recent phylogenomic data sets21, 22, 24, 28, 113. There are three major phyla of extant deuterostomes, The deuterostome context of chordate origins Christopher J. Lowe et al. Nature 520, 456–465 (23 April 2015)