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Ctenophores are direct developers that reproduce continuously beginning very early after hatching - PubMed

  • ️Sat Jan 01 2022

Ctenophores are direct developers that reproduce continuously beginning very early after hatching

Allison Edgar et al. Proc Natl Acad Sci U S A. 2022.

Abstract

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.

Keywords: Mnemiopsis leidyi; ctenophore; dissogeny; larval reproduction; life history evolution.

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Conflict of interest statement

The authors declare no competing interest.

Figures

Fig. 1.
Fig. 1.

Appearance of reproductive cydippids’ gonads and progeny. (A) Apical (aboral) view of a reproductively mature cydippid. Four of the eight gonads are visibly enlarged (large arrowheads); the adtentacular (closer to the plane of the tentacles) four gonads are visibly smaller (small arrows). (B) Lateral view of a reproductively mature cydippid. Oral pole faces up. Enlarged adesophageal (orthogonal to the plane of the tentacles) gonads face the viewer. (C) Unenlarged adtentacular gonad under higher magnification (side view). (D) Enlarged adesophageal gonad in the same animal (side view). Arrowhead highlights a visible immature oocyte. (E) Face-on view of a gonad in a live, reproductively active cydippid. (F) High-magnification view of an ovary in a reproductively active cydippid. Arrowheads highlight individual large cells, likely nurse cells. (G) Apical (aboral) view of a live offspring of a cydippid ∼24 hpf. (H) Live offspring of a cydippid ∼24 hpf. Oral pole faces up. Scale bar A, B = 1 mm; scale bar C, D, E, G, and H = 100 µm; scale bar F = 20 µm.

Fig. 2.
Fig. 2.

Daily reproductive output of individual M. leidyi at body size 1 to 8 mm. (A) Histogram of embryos counted in daily observations of 56 individuals from four biological replicates. Numbers above each bar indicate the number of times a given clutch size was produced. (B) Clutch size (embryos per clutch on days when any embryos are produced) increases with parental body size (n = 98 clutches produced by 32 individuals from four biological replicates) when zero spawn days are excluded; the blue line shows the mean, and shading around the line shows the 95% CI. The 7-mm individuals were relatively undersampled, so we believe this to be an outlier. (C) The transition from cydippid to lobate morphology begins ∼2 mm and is apparent by ∼5 mm, which overlaps with the appearance of lobate morphology. Bars in each panel represent 1 mm. (D and E) Staircase graphs showing predicted mean cumulative reproductive output of isolated individuals at body size 1 to 8 mm. (D) Embryos produced. (E) Daily normal hatched offspring produced by 24 hpf. Each colored line represents reproductive output at a different parental body size in millimeters; lines do not represent specific individuals. Specific individuals’ outputs across different body sizes can be seen in

SI Appendix, Fig. S1C

. The hypothesized gap period of 2 to 4 mm is highly sampled in the dataset, but no such pause is apparent. Repeated measures of 68 isolated individuals at various body sizes of 1- to 8-mm diameter, totaling 307 daily observations, from seven biological replicates. (F) The two columns represent the BIC results for all models evaluated in the size experiments shown in D and E; bootstrapping results are in parentheses. The model with the lowest BIC should be understood as the model that most closely represents the generating process given the data; the nonparametric bootstrapping results indicate the uncertainty around selection of that model (

SI Appendix

for model derivation). Abbreviations: bio.rep = biological replicate; tech.rep = technical replicate.

Fig. 3.
Fig. 3.

Environmental temperature affects fecundity, as shown by predicted mean cumulative reproductive output at two temperatures, 20 and 28 °C, indicating  a daily increase from ∼0.88 embryos/parent to ∼2.05 embryos/parent between the two temperatures. Repeated measures of 133 parental cydippids cultured in four groups of 7 to 20 animals from four biological replicates, totaling 63 total daily observations. (A) Reproductive M. leidyi cydippids produce more embryos and (B) more normal 24 hpf offspring when incubated at the warmer temperature. (C) The two columns represent the BIC results for all models evaluated in the temperature experiments shown in A and B; bootstrapping results are in parentheses. The model with the lowest BIC should be understood as the model that most closely represents the generating process given the data; the nonparametric bootstrapping results indicate the uncertainty around selection of that model (

SI Appendix

for model derivation). (D) Per capita fecundity at 20 and 28 °C. Shaded area (transparent) shows the 95% CI; by chance, the CIs of the samples are very closely apposed. Abbreviations: bio.rep = biological replicate; temp = temperature.

Fig. 4.
Fig. 4.

Fecundity increases with culture density. (A and B) Predicted mean cumulative reproductive output at four culture densities (one to eight animals per 50-mL culture). There were 297 individual observations of n = 60 treatment replicates totaling 174 animals from four biological replicates. (C) The two columns represent the BIC results for all models evaluated in the density experiments shown in A and B; bootstrapping results are in parentheses. The model with the lowest BIC should be understood as the model that most closely represents the generating process given the data; the nonparametric bootstrapping results indicate the uncertainty around selection of that model (

SI Appendix

for model derivation). (D) Per capita fecundity for each biological replicate. Shaded area shows SE.

Fig. 5.
Fig. 5.

Rotifer (prey) nutrition affects M. leidyi capacity to spawn at small sizes (1 to 3 mm). Repeated measures for 8 d of n = 148 animals in cultures of 12 to 20 individuals per treatment from two biological replicates, totaling 64 daily observations. (A) Predicted mean cumulative reproductive output of embryos at four dietary levels of DHA. (B) Predicted mean cumulative reproductive output normal 24 hpf offspring cydippids at four dietary levels of DHA. Dashed line is used where two treatment lines overlap (19.5% in B and D) to facilitate visualization. (C) Predicted mean cumulative reproductive output of embryos at four dietary levels of total lipids. (D) Predicted mean cumulative reproductive output normal 24 hpf offspring cydippids at four dietary levels of total lipids. (E) The two columns represent the BIC results for all models evaluated in the diet experiments shown in A–D; bootstrapping results are in parentheses. The model with the lowest BIC should be understood as the model that most closely represents the generating process given the data; the nonparametric bootstrapping results indicate the uncertainty around selection of that model (

SI Appendix

for model derivation). Abbreviations: bio.rep = biological replicate; num = number; DHA = docosahexaenoic acid; parental.dpf = parental days post-fertilization (parental age).

Fig. 6.
Fig. 6.

Revised model for ctenophore sexual maturation. (A) Ctenophores do not have two separate phases of reproduction as described in previous literature (dissogeny model). Rather, hatched ctenophores become fertile early and slowly increase their reproductive output (continuous reproduction model). (B) Several variables tested affect fecundity similarly in small-size M. leidyi as in published reports on large-size animals. These reproductive characteristics—responsiveness to nutrition, temperature, culture density, continuous and gradually increasing reproductive capacity, and the commonness of small-size spawning—all clearly suggest that M. leidyi are functionally adult from a body size ⪆ 1 mm, regardless of morphology. (C) Small-size reproduction mapped onto a cladogram of the Ctenophora. Tree topology based on Whelan et al. (22). Pink boxes containing a genus name indicate a branch with one or more species that have been shown to reproduce at a small size (∼0.5 to 1 mm) (16, 19, 20, 46); the pink circle indicates the most recent common ancestor of these taxa. Green bars indicate lineages with at least some species exhibiting morphologies other than cydippid at some developmental stage, as reconstructed in Whelan et al. (22). Beroids do not have a cydippid form at any stage. Reproduction at similarly small sizes has not been ruled out in the other ctenophore lineages. Abbreviations: DHA = docosahexaenoic acid; EFAs = essential fatty acids.

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