skip to main content


Title: The sex lives of ctenophores: the influence of light, body size, and self-fertilization on the reproductive output of the sea walnut, Mnemiopsis leidyi

Ctenophores (comb jellies) are emerging as important animals for investigating fundamental questions across numerous branches of biology (e.g., evodevo, neuroscience and biogeography). A few ctenophore species including, most notably,Mnemiopsis leidyi, are considered as invasive species, adding to the significance of studying ctenophore ecology. Despite the growing interest in ctenophore biology, relatively little is known about their reproduction. Like most ctenophores,M. leidyiis a simultaneous hermaphrodite capable of self-fertilization. In this study, we assess the influence of light on spawning, the effect of body size on spawning likelihood and reproductive output, and the cost of self-fertilization on egg viability inM. leidyi. Our results suggest thatM. leidyispawning is more strongly influenced by circadian rhythms than specific light cues and that body size significantly impacts spawning and reproductive output.Mnemiopsis leidyiadults that spawned alone produced a lower percentage of viable embryos versus those that spawned in pairs, suggesting that self-fertilization may be costly in this species. These results provide insight into the reproductive ecology ofM. leidyiand provide a fundamental resource for researchers working with them in the laboratory.

 
more » « less
NSF-PAR ID:
10015602
Author(s) / Creator(s):
 ;  
Publisher / Repository:
PeerJ
Date Published:
Journal Name:
PeerJ
Volume:
4
ISSN:
2167-8359
Page Range / eLocation ID:
e1846
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. A substantial body of literature reports that ctenophores exhibit an apparently unique life history characterized by biphasic sexual reproduction, the first phase of which is called larval reproduction or dissogeny. Whether this strategy is plastically deployed or a typical part of these species’ life history was unknown. In contrast to previous reports, we show that the ctenophore Mnemiopsis leidyi does not have separate phases of early and adult reproduction, regardless of the morphological transition to what has been considered the adult form. Rather, these ctenophores begin to reproduce at a small body size and spawn continuously from this point onward under adequate environmental conditions. They do not display a gap in productivity for metamorphosis or other physiological transition at a certain body size. Furthermore, nutritional and environmental constraints on fecundity are similar in both small and large animals. Our results provide critical parameters for understanding resource partitioning between growth and reproduction in this taxon, with implications for management of this species in its invaded range. Finally, we report an observation of similarly small-size spawning in a beroid ctenophore, which is morphologically, ecologically, and phylogenetically distinct from other ctenophores reported to spawn at small sizes. We conclude that spawning at small body size should be considered as the default, on-time developmental trajectory rather than as precocious, stress-induced, or otherwise unusual for ctenophores. The ancestral ctenophore was likely a direct developer, consistent with the hypothesis that multiphasic life cycles were introduced after the divergence of the ctenophore lineage. 
    more » « less
  2. Despite long-standing experimental interest in ctenophores due to their unique biology, ecological influence and evolutionary status, previous work has largely been constrained by the periodic seasonal availability of wild-caught animals and difficulty in reliably closing the life cycle. To address this problem, we have developed straightforward protocols that can be easily implemented to establish long-term multigenerational cultures for biological experimentation in the laboratory. In this protocol, we describe the continuous culture of the Atlantic lobate ctenophore Mnemiopsis leidyi. A rapid 3-week egg-to-egg generation time makes Mnemiopsis suitable for a wide range of experimental genetic, cellular, embryological, physiological, developmental, ecological and evolutionary studies. We provide recommendations for general husbandry to close the life cycle of Mnemiopsis in the laboratory, including feeding requirements, light-induced spawning, collection of embryos and rearing of juveniles to adults. These protocols have been successfully applied to maintain long-term multigenerational cultures of several species of pelagic ctenophores, and can be utilized by laboratories lacking easy access to the ocean. We also provide protocols for targeted genome editing via microinjection with CRISPR–Cas9 that can be completed within ~2 weeks, including single-guide RNA synthesis, early embryo microinjection, phenotype assessment and sequence validation of genome edits. These protocols provide a foundation for using Mnemiopsis as a model organism for functional genomic analyses in ctenophores. 
    more » « less
  3. Abstract

    Lobate ctenophores are often numerically dominant members of oceanic epipelagic and midwater ecosystems. Despite this, little is known about their trophic ecology. Multiple, co‐occurring species are often found in these ecosystems and appear to feed similarly via feeding currents that entrain prey. We quantified the hydrodynamics, morphology, and behavior of four co‐occurring, cosmopolitan lobate species (Eurhamphaea vexilligera,Ocyropsis crystallina,Bolinopsis vitrea, andLeucothea multicornis) to evaluate whether their feeding mechanics lead to differential feeding rates and prey selection. We compared the feeding characteristics of these four oceanic species to the coastal lobate ctenophore,Mnemiopsis leidyi, which is known as a voracious zooplanktivore. We found that despite their morphological diversity, the five lobate species used the same mechanism to generate their feeding current—the hydrodynamics of their feeding currents were similarly laminar and with very low fluid deformation rates. Despite having similar feeding current traits, the species had different in situ swimming behaviors and feeding postures. We show that these different behaviors and postures lead to different prey encounter rates and that several of the oceanic species have the potential to feed at rates similar to or greater thanM. leidyi. As such, the individual and combined trophic impact of oceanic lobate ctenophores is likely to be much greater than previously predicted.

     
    more » « less
  4. Abstract

    Ctenophora is an early‐branching basal metazoan lineage, which may have evolved neurons and muscles independently from other animals. However, despite the profound diversity among ctenophores, basal neuroanatomical data are limited to representatives of two genera. Here, we describe the organization of neuromuscular systems in eight ctenophore species focusing onEuplokamis dunlapae—the representative of the lineage sister to all other ctenophores. Cydippids (Hormiphora hormiphoraandDryodora glandiformis) and lobates (Bolinopsis infundibulumandMnemiopsis leidyi) were used as reference platforms to cover both morphological and ecological diversity within the phylum. We show that even with substantial environmental differences, the basal organization of neural systems is conserved among ctenophores. In all species, we detected two distributed neuronal subsystems: the subepithelial polygonal network and the mesogleal elements. Nevertheless, each species developed specific innovations in neural, muscular, and receptor systems. Most notableEuplokamis‐specific features are the following: (a) Comb nerves with giant axons. These nerves directly coordinate the rapid escape response bypassing the central integrative structure known as the aboral sensory organ. (b) Neural processes in tentacles along the rows of “boxes” providing structural support and located under striated muscles. (c) Radial muscles that cross the mesoglea and connect the outer wall to the aboral canal. (d) Flat muscles, encircling each meridional canal. Also, we detected a structurally different rectangular neural network in the feeding lobes of Lobata (Mnemiopsis/Bolinopsis) but not in other species. The described lineage‐specific innovations can be used for future single‐cell atlases of ctenophores and analyses of neuronal evolution in basal metazoans.

     
    more » « less
  5. Abstract

    Ctenophores are descendants of an early branching basal metazoan lineage, which may have evolved neurons and muscles independently from other animals.Mnemiopsisis one of the important reference ctenophore species. However, little is known about its neuromuscular organization. Here, we mapped and tracked the development of the neural and muscular elements in the early hatching cydippid larvae, as well as adultMnemiopsis leidyi. The overall development of the neuromuscular system inMnemiopsiswas very similar toPleurobrachia bachei, although inMnemiopsisthe entire process occurred significantly faster. The subepithelial neural cells were observed immediately after hatching. This population consisted of a dozen of separated individual neurons with short neurites. In about 2 days, when their neurites grew significantly longer and connected to their neighbors, they began to form a canonical polygonal subepithelial network. Mesogleal neural elements prominent in all studied adult ctenophores were not detectable inMnemiopsislarvae but were clearly labeled in closely related Lobata speciesBolinopsis infundibulum. Hatched larvae also had putative mechanoreceptors with long stereocilia and approximately two dozen muscle cells. In adultMnemiopsis,the feeding lobes and auricles contained two distinct populations of neurons and neural ensembles that were not observed in other ctenophore lineages and likely represented elaborate neuronal innovations characteristic for the clade Lobata and their lifestyles.

     
    more » « less