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A phylum-wide survey reveals multiple gains of regenerative ability in

nemerteans

Conference Paper · January 2015

DOI: 10.13140/RG.2.1.5183.9768

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Eduardo E Zattara Jon Norenburg

National Scientific and Technical Research Council Smithsonian Institution
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 A phylum-wide survey reveals
multiple gains of regeneration in
Nemerteans

Eduardo E. Zattara1,2, Jon L. Norenburg1 and Alexa E. Bely2

Invertebrate Zoology, National Museum of Natural History,
Smithsonian Institution
Department of Biology, College of Mathematics, Computer and Life Sciences,
University of Maryland, College Park
The evolution of novelty
• How do novel traits evolve?
• Novel trait evolution is found at many levels
• Novel genes/proteins and protein functions
• Novel gene regulatory pathways
• Novel cell types and cell-cell interactions
• Novel morphological structures
• Novel developmental trajectories
The evolution of novel developmental trajectories
• Examples of developmental
trajectories
• Embryogenesis
Zygote
• Post-embryonic development Larva
• Indirect (metamorphic) Embryogenesis Embryogenesis
development (direct) (indirect)
• Asexual agametic reproduction
Adult
• Regeneration

Agametic reproduction
Regeneration
 Is regeneration a novel trajectory?
• Regeneration abilities
vary across metazoans
• Surveys that are too
coarse-grained fail to
resolve polarity of
change
• Gains?
• Losses?
• Ancestral trait state?

Zattara 2012
Regeneration in the phylum Nemertea
Hubrechtidae sp.883

Cephalothrix spiralis

Cerebratulus lineolatus Baseodiscus delineatus

Ramphogordius sanguineus

Poseidonemertes sp.

Nemertopsis bivittata Zygonemertes albida

Regeneration in the phylum Nemertea
• Acoelomate, no hard skeleton
• Highly muscular
• Body covered in cilia
• Unique proboscis apparatus
• Central nervous system, four-lobbed brain, lateral nerve cords
• Primarily benthic marine worms
• ~900-1200 described species

Serotonin
Acetyl-tubulin
DNA Ramphogordius sanguineus (Heteronemertea: Lineidae)
 Regeneration in the phylum Nemertea

• Reports for only a few

families
• There is within family
variation in
regenerative ability
• Gains?
• Losses?
• Ancestral trait state?

Bely, Zattara & Sikes 2015

Surveying regeneration across Nemertea
• Survey methodology
• Pack (or ask)
• Catch
• Cut
• Watch
• Sequence
• DNA markers
• Mitochondrial: COI (L/H) and 16S
• Nuclear: 18S and 28S
• MAFFT alignment + manual curation
• Phylogenetic inference using MrBayes, GARLI and RAxML
 Anterior regeneration ability varies across species
PALEONEMERTEANS: variation in head regeneration ability
Cephalothrix spiralis and C. simula

Tubulanus sexlineatus and T. polymorphus

27 dpa
Anterior regeneration ability varies across species
HOPLONEMERTEANS: NO head regeneration ability
Zygonemertes albidus

Nemertopsis bivitatta

17 dpa

Poseidonemertes sp.

15 dpa

2 dpa
 Anterior regeneration ability varies across species
HETERONEMERTEANS: much variation in head regeneration ability
Ramphogordius sanguineus

Baseodiscus Cerebratulus
Ramphogordius lacteus Lineus ruber Lineus viridis delineatus lineolatus
~ 20 dpa 30 dpa > 120 dpa
Phylogenetic inference results
• 117 new sequences from 32 worm samples
• Concatenated dataset ~10kbp long
• Tree topologies inferred using different methods (MrBayes, GARLI,
RAxML) were mostly similar
• Tree topologies mostly congruent with latest multigene published
phylogenies (Thollesson & Norenburg 2003; Andrade et al. 2011,
2013)
• Constraining inference to fit with published phylogenies did not
change noticeably ancestral character estimation analyses.
Distribution of regeneration and ancestral character estimation

• MrBayes phylogram

PALEO
(1.25E6 gens.) recovers
main groups

HOPLO
• Trait mapping shows
posterior regeneration
always present, but
anterior regeneration
varies
• Ancestral character
estimation yields 4 gains
of head regeneration

HETERO
• No loss of head
regeneration found
 There is great variability in survival and regeneration timing

No head reg.; killed

K
No head reg.; died
†
Full head reg.

Anterior amputation result

Assessing regenerative ability across nemerteans
• Posterior regeneration is present across the whole phylum
• Head regeneration newly described for 4 nemertean species
• First cases in Paleonemertea
• Ancestral character estimation suggests at least 4 independent gains
of head regeneration
• Lack of head regeneration in the sister species of “regeneration
champion” Ramphogordius sanguineus suggest recent gain of this
trait.
Final remarks
• The basal nemerteans were likely able to regenerate the tail, but not
the head.
• Head regeneration has evolved multiple times within the phylum.
• The species pair Ramphogordius lacteus and R. sanguineus can be
used as a study system to understand the genetic and developmental
underpinnings of regeneration gains.
• Deeper taxonomic sampling is fundamental to correctly estimate
character gains and losses during evolution of a lineage.
 Acknowledgments
• Additional worm collection, experiments and shipping
• Fernando Ángel Fernández-Alvarez (Institut de Ciències del Mar, CSIC,
Barcelona, Spain)
• Chris Laumer (Harvard University, Organismic and Evolutionary Biology, USA)
• Svetlana Maslakova, Terra Hiebert (Oregon Institute of Marine Biology, USA)
• Carlos Vives, Pia Floria
• Worm sequencing and bioinformatics
• Jeff Hunt, Herman Wirshing, Francesca Leasi, Matt Kweskin, Lee Weigt
(Laboratories of Analytical Biology, NMNH, SI)

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