Morphogenesis and phenotypic divergence in two developmental morphs of <i>Streblospio benedicti</i> (Annelida, Spionidae)

Gibson, Glenys D.; MacDonald, Kristen; Dufton, Megan

doi:10.1111/j.1744-7410.2010.00213.x

Cited by 28 publications

(34 citation statements)

References 29 publications

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“…the presence of different developmental types in the same species, for example in Annelida and Mollusca. In the annelid family Spionidae, Streblospio benedicti [140] two morphs are found one of which deposits small eggs developing into planktotrophic trochophores, whereas the other morph deposits large eggs developing into lecithotrophic (or facultatively planktotrophic) larvae. Boccardia proboscidea [141] deposits egg masses with each egg capsule containing many eggs, some of which develop into larvae which hatch as planktotrophic larvae, whereas other embryos feed on nurse eggs and hatch as advanced larvae or small juveniles.…”

Section: Reviewmentioning

confidence: 99%

Life cycle evolution: was the eumetazoan ancestor a holopelagic, planktotrophic gastraea?

Nielsen

2013

BMC Evol Biol

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BackgroundTwo theories for the origin of animal life cycles with planktotrophic larvae are now discussed seriously: The terminal addition theory proposes a holopelagic, planktotrophic gastraea as the ancestor of the eumetazoans with addition of benthic adult stages and retention of the planktotrophic stages as larvae, i.e. the ancestral life cycles were indirect. The intercalation theory now proposes a benthic, deposit-feeding gastraea as the bilaterian ancestor with a direct development, and with planktotrophic larvae evolving independently in numerous lineages through specializations of juveniles.ResultsInformation from the fossil record, from mapping of developmental types onto known phylogenies, from occurrence of apical organs, and from genetics gives no direct information about the ancestral eumetazoan life cycle; however, there are plenty of examples of evolution from an indirect development to direct development, and no unequivocal example of evolution in the opposite direction. Analyses of scenarios for the two types of evolution are highly informative. The evolution of the indirect spiralian life cycle with a trochophora larva from a planktotrophic gastraea is explained by the trochophora theory as a continuous series of ancestors, where each evolutionary step had an adaptational advantage. The loss of ciliated larvae in the ecdysozoans is associated with the loss of outer ciliated epithelia. A scenario for the intercalation theory shows the origin of the planktotrophic larvae of the spiralians through a series of specializations of the general ciliation of the juvenile. The early steps associated with the enhancement of swimming seem probable, but the following steps which should lead to the complicated downstream-collecting ciliary system are without any advantage, or even seem disadvantageous, until the whole structure is functional. None of the theories account for the origin of the ancestral deuterostome (ambulacrarian) life cycle.ConclusionsAll the available information is strongly in favor of multiple evolution of non-planktotrophic development, and only the terminal addition theory is in accordance with the Darwinian theory by explaining the evolution through continuous series of adaptational changes. This implies that the ancestor of the eumetazoans was a holopelagic, planktotrophic gastraea, and that the adult stages of cnidarians (sessile) and bilaterians (creeping) were later additions to the life cycle. It further implies that the various larval types are of considerable phylogenetic value.

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Section: Reviewmentioning

confidence: 99%

Life cycle evolution: was the eumetazoan ancestor a holopelagic, planktotrophic gastraea?

Nielsen

2013

BMC Evol Biol

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“…As one of the most common polychaete species on both coasts of North America, and also due to poecilogonous ability to produce planktotrophic and lecithotrophic larvae, S. benedicti became a subject of numerous studies on ecology and reproductive biology (e.g. Levin & Huggett, 1991;Mccain, 2008;Gibson et al, 2010). The other two species have been less thoroughly studied and morphological differences between them have remained uncertain.…”

Section: Remarksmentioning

confidence: 99%

Records of Polydora cornuta and Streblospio gynobranchiata (Annelida, Spionidae) from the Black Sea

Radashevsky

Селіфонова

2013

Medit. Mar. Sci.

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Two spionid polychaetes, Polydora cornuta and Streblospio gynobranchiata, were identified in benthic samples collected in the northern Black Sea and adjacent waters. These species have earlier been classified as the worst invaders in soft bottom communities in the Mediterranean Sea. Polydora cornuta had been previously misidentified and widely reported from the Black Sea and the Sea of Azov as P. ciliata, P. ciliata limicola and P. limicola. Streblospio gynobranchiata is a new invader currently extending its distribution into the Mediterranean, Black and Caspian Seas. Morphology, diagnostic characters and biology of the species are discussed and the history of their records in the Mediterranean, Black and Caspian Seas and the Sea of Azov is reviewed.

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“…Lecithotrophic mothers produce large (~200um) eggs that develop into larvae that do not require exogenous food and quickly leave the water column as benthic juveniles. These larvae lack swimming chaetae and a second type of larva-specific morphological structure, anal cirri containing bacillary cells, which are distinctive rhabdomeric cells of unknown function 22 (Fig 1a). There are also differences during embryogenesis 23 and organogenesis 22,24 , where accelerated development of juvenile features and truncated development of larval features occurs in lecithotrophs .…”

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Decoupled Maternal and Zygotic Genetic Effects Shape the Evolution of Development

Zakas

Deutscher

Kay

et al. 2017

Preprint

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Many animals develop indirectly via a larval stage that is morphologically and ecologically distinct from its adult form. Hundreds of lineages across animal phylogeny have secondarily lost larval forms, instead producing offspring that directly develop into adult form without a distinct larval ecological niche 1-7 . Indirect development in the sea is typically planktotrophic: females produce large numbers of small offspring that require exogenous planktonic food to develop before metamorphosing into benthic juveniles. Direct development is typically lecithotrophic: females produce a smaller number of larger eggs, each developing into a juvenile without the need for larval feeding, provisioned by yolk. Evolutionary theory suggests that these alternative developmental strategies represent stable alternative fitness peaks, while intermediate states are disfavored 4,8-11 . Transitions from planktotrophy to lecithotrophy thus require crossing a fitness valley and represent radical and coordinated transformations of life-history, fecundity, ecology, dispersal, and development 7,12-16 . Here we dissect this transition in Streblospio benedicti, the sole genetically tractable species that harbors both states as heritable variation [17][18][19] . We identify large-effect loci that act maternally to influence larval size and independent, unlinked large-effect loci that act zygotically to affect discrete aspects of larval morphology. Because lecithotrophs and planktotrophs differ in both size and morphology, the genetic basis of larval form exhibits strong maternal-by-zygotic epistasis for fitness 20 . The fitness of zygotic alleles depends on their maternal background, creating a positive frequency-dependence that may homogenize local populations. Developmental and population genetics interact to shape larval evolution.Streblospio benedicti females fall into two classes exhibiting classic life-history tradeoffs: Planktotrophic mothers produce small (~100um) eggs that develop into obligately feeding larvae that spend weeks in the plankton. These larvae are pelagic and grow larva-specific swimming chaetae that are thought to deter predation 21 (Fig 1a). Lecithotrophic mothers produce large (~200um) eggs that develop into larvae that do not require exogenous food and quickly leave the water column as benthic juveniles. These larvae lack swimming chaetae and a second type of larva-specific morphological structure, anal cirri containing bacillary cells, which are distinctive rhabdomeric cells of unknown function 22 (Fig 1a). There are also differences during embryogenesis 23 and organogenesis 22,24 , where accelerated development of juvenile features and truncated development of larval features occurs in lecithotrophs . Despite these developmental and larval differences, adults are indistinguishable at the level of gross morphology. Unlike examples of polyphenism, environmental input does not substantially alter egg size or subsequent offspring type 25,26 . S. benedicti is common throughout North American estuaries, but local p...

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Morphogenesis and phenotypic divergence in two developmental morphs of Streblospio benedicti (Annelida, Spionidae)

Cited by 28 publications

References 29 publications

Life cycle evolution: was the eumetazoan ancestor a holopelagic, planktotrophic gastraea?

Life cycle evolution: was the eumetazoan ancestor a holopelagic, planktotrophic gastraea?

Records of Polydora cornuta and Streblospio gynobranchiata (Annelida, Spionidae) from the Black Sea

Decoupled Maternal and Zygotic Genetic Effects Shape the Evolution of Development

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