The active evolutionary lives of echinoderm larvae

Raff, Rudolf A.; Byrne, Maria

doi:10.1038/sj.hdy.6800866

Cited by 127 publications

(102 citation statements)

References 68 publications

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“…The planktotrophic larva is regarded as the ancestral larval type for extant Echinodermata, and after 500 million years of larval evolution (Raff and Byrne 2006), we find that 68% of species with known development have the derived, lecithotrophic larval type (see the Appendix). We hypothesize that the evolutionary trend in the Echinodermata is toward a buffered ''lower-risklower-gain'' strategy of direct-developing lecithotrophic larvae.…”

Section: Three Generalized Patterns and Hypothesized Causes For Largementioning

confidence: 99%

A boom–bust phylum? Ecological and evolutionary consequences of density variations in echinoderms

Uthicke

Schaffelke

Byrne

2009

Ecological Monographs

376

245

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Abstract. Echinoderms play a key role in structuring many marine ecosystems and are notorious for large population density variations in so-called ''outbreak'' or ''dieoff'' events. In a review of this phenomenon, we assess the causal factors and ecological and evolutionary consequences. We identified 28 species (6 Asteroidea, 8 Echinoidea, 10 Holothuroidea, 4 Ophiuroidea) that exhibit large (more than two population doublings or halvings) population density changes. Three generalized patterns were identified and named for exemplary species:(1) rapid decreases followed by no or slow recovery (Diadema-Paracentrotus Model), (2), rapid increase and apparent stability at a new population density (Amperima-Amphiura Model), and (3) population density fluctuations (Acanthaster-Asterias Model). Echinoderms identified were distributed from the shallow intertidal to the deep sea, and from tropical to temperate regions. In most cases, significant impacts on the respective ecosystems were observed. The most striking similarity among all species identified was possession of the ancestral-type planktotrophic larva. This larval type was significantly overrepresented in species identified within the Asteroidea, Echinoidea, Holothuroidea, and for the combined data set. We suggest three main factors that render a life history with planktotrophic larvae a high-risk-high-gain strategy: (1) a strong nonlinear dependency of larval production on adult densities (Allee effects), (2) a low potential for compensatory feedback mechanisms, and (3) an uncoupling of larval and adult ecology. The alternative (derived) lecithotrophic larva occurs in 68% of recent echinoderm species, suggesting an evolutionary trend toward this larval type. Lecithotrophic development represents a more buffered life history because compensatory feedback between adult densities and larval output is likely to be more efficient. For lecithotrophic developers, direct nutritive coupling from adult to larva to the early benthic juvenile provides a buffer against starvation. Lecithotrophic larvae are independent of the vagaries of planktonic food supply, and their short planktonic duration may promote local recruitment. Anthropogenic influences contributed to the population density variations in most cases, including increased primary productivity through eutrophication or global change, disease, overfishing, and species introductions. We suggest that anthropogenic disturbance, through its influence on the frequency and/or amplitude of echinoderm population density changes, may go beyond present ecosystem impacts and alter future evolutionary trends.

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Section: Three Generalized Patterns and Hypothesized Causes For Largementioning

confidence: 99%

A boom–bust phylum? Ecological and evolutionary consequences of density variations in echinoderms

Uthicke

Schaffelke

Byrne

2009

Ecological Monographs

376

245

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“…A second type of larval evolution is that of the various non-planktotrophic derivatives of larvae in various clades (e.g. snails, Collin 2004; starfish and sea urchins, Raff & Byrne 2006). In many taxa, planktonic feeding larvae have given rise to non-feeding direct-developing planktonic or brooded larvae, and even viviparous larvae.…”

Section: Continuing Gene Co-option In Larval Evolutionmentioning

confidence: 99%

“…Some feeding structures, such as the larval arms and gut, are lost; nonetheless, developmental features retain a high degree of complexity and dramatic novel features have appeared. These include changes in oogenesis and spermatogenesis, maternal embryonic axis determination, cleavage pattern, cell embryonic lineages, and heterochronies in larval gene expression and morphogenetic events (Raff & Byrne 2006). The details, described elsewhere, show that rapid and profound evolutionary changes in larval development occur.…”

Section: Continuing Gene Co-option In Larval Evolutionmentioning

confidence: 99%

Origins of the other metazoan body plans: the evolution of larval forms

Raff

2008

Phil. Trans. R. Soc. B

139

103

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Bilaterian animal body plan origins are not solely about adult forms. Most animals have larvae with body plans, ontogenies and ecologies distinct from adults. There are two primary hypotheses for larval origins. The first hypothesis suggests that the first animals were small pelagic forms similar to modern larvae, with adult bilaterian body plans evolved subsequently. The second hypothesis suggests that adult bilaterian body plans evolved first and that larval body plans arose by interpolation of features into direct-developing ontogenies. The two hypotheses have different consequences for understanding parsimony in evolution of larvae and of developmental genetic mechanisms. If primitive metazoans were like modern larvae and distinct adult forms evolved independently, there should be little commonality of patterning genes among adult body plans. However, sharing of patterning genes is observed. If larvae arose by co-option of adult bilaterian-expressed genes into independently evolved larval forms, larvae may show morphological convergence, but with distinct patterning genes, and this is observed. Thus, comparative studies of gene expression support independent origins of larval features. Precambrian and Cambrian embryonic fossils are also consistent with direct development of the adult as being primitive, with planktonic larvae arising during the Cambrian. Larvae have continued to co-opt genes and evolve new features, allowing study of developmental evolution.

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“…One main question regarding larval form is whether similarities in larval morphology are phylogenetically linked or if the body plans of larvae are free to evolve, arriving at similar morphologies based on convergent selective pressures (McEdward and Janies, 1993;Strathmann and Eernisse, 1994;Wray, 2002;Santagata, 2004;Raff and Byrne, 2006). Several investigations have concluded that the transition from a feeding to a nonfeeding larva (or vice versa) is a common evolutionary switch among marine invertebrates having no significant phylogenetic signal (Hart et al, 1997;Duda and Palumbi, 1999;Nü tzel et al, 2006).…”

Section: Introductionmentioning

confidence: 99%

The morphology and evolutionary significance of the ciliary fields and musculature among marine bryozoan larvae

Santagata

2007

Journal of Morphology

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Despite the embryological and anatomical disparities present among lophotrochozoan phyla, there are morphological similarities in the cellular arrangements of ciliated cells used for propulsion among the nonfeeding larval forms of kamptozoans, nemerteans, annelids, mollusks, and bryozoans. Evaluating whether these similarities are the result of convergent selective pressures or a shared (deep) evolutionary history is hindered by the paucity of detailed cellular information from multiple systematic groups from lesser-known, and perhaps, basal evolutionary phyla such as the Bryozoa. Here, I compare the ciliary fields and musculature among the major morphological grades of marine bryozoan larvae using light microscopy, SEM, and confocal imaging techniques. Sampling effort focused on six species from systematic groups with few published accounts, but an additional four well-known species were also reevaluated. Review of the main larval types among species of bryozoans and these new data show that, within select systematic groups of marine bryozoans, there is some conservation of the cellular arrangement of ciliary fields and larval musculature. However, there is much more morphological diversity in these structures than previously documented, especially among nonfeeding ctenostome larval types. This structural and functional diversification reflects species differences in the orientation of the apical disc during swimming and crawling behaviors, modification of the presumptive juvenile tissues, elongation of larval forms in the aboral-oral axis, maximizing the surface area of cell types with propulsive cilia, and the simplification of ciliary fields and musculature within particular lineages due to evolutionary loss. Considering the embryological origins and functional plasticity of ciliated cells within bryozoan larvae, it is probable that the morphological similarities shared between the coronal cells of bryozoan larvae and the prototrochal cells of trochozoans are the result of convergent functional solutions to swimming in the plankton. However, this does not rule out cell specification pathways shared by more closely related spiralian phyla. Overall, among the morphological grades of larval bryozoans, the structural variation and arrangement of the main cell groups responsible for ciliary propulsion have been evolutionarily decoupled from the more divergent modifications of larval musculature. The structure of larval ciliary fields reflects the functional demands of swimming and substrate exploration behaviors before metamorphosis, but this is in contrast to the morphology of larval musculature and presumptive juvenile tissues that are linked to macroevolutionary differences in morphogenetic movements during metamorphosis.

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The active evolutionary lives of echinoderm larvae

Cited by 127 publications

References 68 publications

A boom–bust phylum? Ecological and evolutionary consequences of density variations in echinoderms

A boom–bust phylum? Ecological and evolutionary consequences of density variations in echinoderms

Origins of the other metazoan body plans: the evolution of larval forms

The morphology and evolutionary significance of the ciliary fields and musculature among marine bryozoan larvae

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