Evolution of Life Histories: Echinoderms as Model Systems

Types of development in sea stars The typical sea star larva is the bipinnaria, it drifts in the water and feeds on algae : planktotrophic Planktotrophic development is the ancestral type. Other types of development evolved from planktotrophic Some species have swimming larvae that rely on maternal yolk for food: lecithotrophic Other species protect (brooding) their eggs and young until a juvenile stage is reached

0.5 mm 1.0 mm 0.2 mm (in maternal brood chamber) 1 mm 2 mm 0.5 mm 2.5 mm 1.5 mm

Evolution of developmental strategies depends on the balance between many selective forces: Think about evolution in terms of Trade OFFS Planktotrophic Larvae ------------------- low investment/egg high fecundity wide dispersal must find food long development very high mortality Lecithotrophic larvae ------------------- investment is higher lower fecundity limited dispersal no food needed limited duration some mortality. Protected development ------------------- very high investment very low fecundity no dispersal no food needed parent protection low mortality

Studies of Evolution of Development Stepwise transition from indirect to direct larval development in sea urchins Studies of Evolution of Development In Sea Urchins The first step involves the switch from obligatory to facultative feeding The second step involves the loss of the ability to feed (but vestigial structures may remain) 3. The third step involves the minimizing of the amount of time required to complete metamorphosis (regulatory genes) Complete loss of structures associated with feeding in the larvae Schmoo from Lil Abner cartoon

Studies of Evolution of Development In Sea Urchins Australian Sea urchins of the genus Heliocidaris

Australian Sea urchins of the genus Heliocidaris Gastrula pluteus larva pluteus with rudiment

Egg Diam (microns) 90 430 Days to juvenile 42 4 Egg biochem Protein Heliocidaris tuberculata Heliocidaris erythrogramma Two strikingly different pathways of early development lead to a similar outcome H.t. H.e Egg Diam (microns) 90 430 Days to juvenile 42 4 Egg biochem Protein rich Lipid Larva Feeding, complete relic tiny enormous

Fate Map Neurons Gut Skeletal Coelom Ectoderm Stipple: non-ectoderm N : Neurons C : Coelom E : Ectoderm G: Gut P : Pigment S : Skeletogenic Heterotopies and Heterochronies Big egg Little egg Neurons Gut Skeletal Coelom Ectoderm Divisions 1 2 3 “Modifications are not limited to deletions in the larval program of development but profoundly affect the embryonic origin of adult tissues and structures as well” Wray & Raff, 1991

Heterochronies in Wnt genes and juvenile rudiment development - Wnt genes important regulatory transcription factors for signaling pathways in animal development. In Echinoderms, Wnt genes are expressed in tissues that form the early adult rudiment and the adult radial nervous system. Wnt expression peaks at 28 days in Ht feeding larvae and 24 hrs in He nonfeeding larvae Wnt expression domains do not change (no heterotopies) but are accelerated in rudiment both in absolute time as well as relative to the formation of other larval structures; this is part of overall earlier onset of development of adult structures. They parallel the accelerated rate of development seen in embryonic and larval tissues.

Studies of Heliocidaris Hybrids by Raff et al. 1999 Reciprocal crosses H.e. eggs x Ht sperm H.t. eggs x He sperm

Studies of Heliocidaris Hybrids by Raff et al. 1999 H. “tiny” eggs x H. “enormous” sperm results in a lethal hybrid cross due to loss of larval polarity (at gastrulation) … Explain? Gastrulation is first stage where bilateral symmetry is established In Ht and other species with feeding larva only the A-V axis is established maternally; other axes are determined zygotically. So the sperm provides information that is essential to development of other (bilateral) axes. In He, all of the axes must be determined maternally; sperm no longer provide information relevant to larval polarity.

Studies of Heliocidaris Hybrids by Raff et al. 1999 H. t. eggs x H. e. sperm results in a lethal hybrid cross due to loss of larval polarity (at gastrulation) H. ‘tiny’ sperm x H. “enormous” eggs indirect developing paternal influence on direct developing egg results in a novel ontogenetic species

Explain…. H. tuberculata sperm x H. erythrogrammica eggs Formation of a complete gut with surface connections Spicules Development of the adult rudiment within a vestibule on the left side of the mouth Pluteus arms (feeding structures) and a complete ciliary band that lies between the mouth and anus Ectodermal territories are restored Hybrid Larva Explain….

Explain? Indicates a strong paternal role in determination of ectodermal territory and the feeding structures they form

Summary of Hybridization Studies Ht (m) x He (f) hybrids produced a novel synthetic morphology  Indicates that some key aspects of development, particularly the feeding structures are of paternal origin (I.e. the sperm).  The genes for oral ectoderm, digestive system etc. are no longer expressed in He sperm Ht x He (m) fertilization (when successful) resulted in a developmental arrest at gastrulation. The developing embryos were unable to establish proper embryonic axes  Changes in how polarity is established took place in the transition from feeding to non feeding; In He the establishment of embryonic polarity (dorsal-ventral axis) is no longer sperm mediated; it is due to maternal patterning.

In Heliocidaris erythrogramma (big eggs) A mosaic of conserved and radically changed developmental features A. Conserved General rules of primary 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) Ferkowicz and Raff 2001 Kaufman and Raff 2003

A mosaic of conserved and radically changed developmental features B. 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. These “heterochronies” have a highly conserved developmental outcome and are part of overall early onset of development of adult structures Ferkowicz and Raff 2001 Kaufman and Raff 2003