Comparison of neuromuscular development in two dinophilid species (Annelida) suggests progenetic origin ofDinophilus gyrociliatus.
BACKGROUND
Several independent meiofaunal lineages are suggested to have originated through progenesis, however, morphological support for this heterochronous process is still lacking. Progenesis is defined as an arrest of somatic development (synchronously in various organ systems) due to early maturation, resulting in adults resembling larvae or juveniles of the ancestors. Accordingly, we established a detailed neuromuscular developmental atlas of two closely related Dinophilidae using immunohistochemistry and CLSM. This allows us to test for progenesis, questioning whether i) the adult smaller, dimorphicDinophilus gyrociliatusresembles a younger developmental stage of the larger, monomorphicD. taeniatusand whether ii) dwarf males ofD. gyrociliatusresemble an early developmental stage ofD. gyrociliatusfemales.


RESULTS
Both species form longitudinal muscle bundles first, followed by circular muscles, creating a grid of body wall musculature, which is the densest in adultD. taeniatus, while the architecture in adult femaleD. gyrociliatusresembles that of prehatchingD. taeniatus. Both species display a subepidermal ganglionated nervous system with an anterior dorsal brain and five longitudinal ventral nerve bundles with six sets of segmental commissures (associated with paired ganglia). Neural differentiation ofD. taeniatusand femaleD. gyrociliatuscommissures occurs before hatching: both species start out forming one transverse neurite bundle per segment, which are thereafter joined by additional thin bundles. WhereasD. gyrociliatusarrests its development at this stage, adultD. taeniatuscondenses the thin commissures again into one thick commissural bundle per segment. Generally,D. taeniatusadults demonstrate a seemingly more organized (= segmental) pattern of serotonin-like and FMRFamide-like immunoreactive elements. The dwarf male ofD. gyrociliatusdisplays a highly aberrant neuromuscular system, showing no close resemblance to any early developmental stage of femaleDinophilus, although the onset of muscular development mirrors the early myogenesis in females.


CONCLUSIONS
The apparent synchronous arrest of nervous and muscular development in adult femaleD. gyrociliatus,resembling the prehatching stage ofD. taeniatus,suggests thatD. gyrociliatushave originated through progenesis. The synchrony in arrest of three organ systems, which show opposing reduction and addition of elements, presents one of the morphologically best-argued cases of progenesis within Spiralia.
Marine Biological Section - Department of Biology, University of Copenhagen, Universitetsparken 4, 2100 Copenhagen, Denmark.
Alexandra
0000-0002-9454-6359
A
Kerbl
Laboratory of Developmental Neurobiology, Koltzov Institute of Developmental Biology RAS, 26 Vavilova Str., Moscow, Russia.
Elizaveta G
EG
Fofanova
Laboratory of Developmental Neurobiology, Koltzov Institute of Developmental Biology RAS, 26 Vavilova Str., Moscow, Russia.|Laboratory of Neurobiology, National Institute of Neurological Disorders and Stroke, NIH, 49 Convent Dr., Bethesda, MD USA.
Tatiana D
TD
Mayorova
Laboratory of Developmental Neurobiology, Koltzov Institute of Developmental Biology RAS, 26 Vavilova Str., Moscow, Russia.
Elena E
EE
Voronezhskaya
Marine Biological Section - Department of Biology, University of Copenhagen, Universitetsparken 4, 2100 Copenhagen, Denmark.
Katrine
0000-0003-0443-4298
K
Worsaae
Ciliation; Interstitial; Meiofauna evolution; Musculature; Nervous system; Paedomorphosis; Sexual dimorphism; Sister species