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The effects of experimentally induced adelphophagy in gastropod embryos.

Thomsen O, Collin R, Carrillo-Baltodano A - PLoS ONE (2014)

Bottom Line: We found an overall increase in shell length and velum diameter when embryos feed on damaged siblings within their capsules.The overall effect of our treatment was small compared to the embryonic growth observed in naturally adelphophagic development.These results suggest that the ability to consume, assimilate, and benefit from yolk and tissue of their siblings is widespread across calyptraeids.

View Article: PubMed Central - PubMed

Affiliation: Smithsonian Tropical Research Institute, Balboa, Ancon, Republic of Panama; Universität Oldenburg, Oldenburg, Germany.

ABSTRACT
Adelphophagy, development where embryos grow large by consuming morphologically distinct nutritive embryos or their own normal siblings is widespread but uncommon among animal phyla. Among invertebrates it is particularly common in some families of marine gastropods and segmented worms, but rare or unknown in other closely related families. In calyptraeid gastropods phylogenetic analysis indicates that adelphophagy has arisen at least 9 times from species with planktotrophic larval development. This pattern of frequent parallel evolution of adelphophagy suggests that the embryos of planktotrophic species might be predisposed to evolve adelphophagy. Here we used embryos of three species of planktotrophic calyptraeids, one from each of three major genera in the family (Bostrycapulus, Crucibulum, and Crepidula), to answer the following 3 questions: (1) Can embryos of species with planktotrophic development benefit, in terms of pre-hatching growth, from the ingestion of yolk and tissue from experimentally damaged siblings? (2) Does ingestion of this material from damaged siblings increase variation in pre-hatching size? and (3) Does this experimentally induced adelphophagy alter the allometry between the velum and the shell, increasing morphological similarity to embryos of normally adelphophagic species? We found an overall increase in shell length and velum diameter when embryos feed on damaged siblings within their capsules. There was no detectable increase in variation in shell length or velum diameter, or changes in allometry. The overall effect of our treatment was small compared to the embryonic growth observed in naturally adelphophagic development. However each embryo in our experiment probably consumed less than one sibling on average, whereas natural adelphophages often each consume 10-30 or more siblings. These results suggest that the ability to consume, assimilate, and benefit from yolk and tissue of their siblings is widespread across calyptraeids.

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Related in: MedlinePlus

A series of video frames of an excapsulated Crepidula cf. marginalis embryo after it has fed for 40 minutes.The anterior opaque area shows yolk accumulated in the esophagus and buccal cavity. In this series a larger particle is transported via a combination of cilia on the food groove and a twitch of the velum, and is added to the yolk accumulated at the mouth.
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pone-0103366-g004: A series of video frames of an excapsulated Crepidula cf. marginalis embryo after it has fed for 40 minutes.The anterior opaque area shows yolk accumulated in the esophagus and buccal cavity. In this series a larger particle is transported via a combination of cilia on the food groove and a twitch of the velum, and is added to the yolk accumulated at the mouth.

Mentions: For the Encapsulated Experiment 6 capsules were removed from the female and each was placed individually in a Petri dish. Three capsules were assigned to the treatment and 3 were assigned to the control (Figure 1). For treated capsules 20–40% of the embryos within a single capsule were killed by applying pressure to the intact capsule with thin flat forceps (Figure 2). Care was taken not to rupture the capsule wall, and any capsules that appeared damaged were discarded. Observation of the treated capsules showed that the small yolk particles were cleared from the capsule fluid within 2–3 hours and that larger fragments took longer to clear (Figure 2). Because the capsules are a closed system, and because undamaged embryos were observed to capture and ingest yolk particles (Figures 3 & 4, Video S1), it seems likely that this material was ingested. For the control group, the intact capsules were each left in a Petri dish without killing any of the embryos. Broods from 9 females were used for C. cf. marginalis, 11 for C. spinosum, and 16 for B. calyptraeformis.


The effects of experimentally induced adelphophagy in gastropod embryos.

Thomsen O, Collin R, Carrillo-Baltodano A - PLoS ONE (2014)

A series of video frames of an excapsulated Crepidula cf. marginalis embryo after it has fed for 40 minutes.The anterior opaque area shows yolk accumulated in the esophagus and buccal cavity. In this series a larger particle is transported via a combination of cilia on the food groove and a twitch of the velum, and is added to the yolk accumulated at the mouth.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC4114838&req=5

pone-0103366-g004: A series of video frames of an excapsulated Crepidula cf. marginalis embryo after it has fed for 40 minutes.The anterior opaque area shows yolk accumulated in the esophagus and buccal cavity. In this series a larger particle is transported via a combination of cilia on the food groove and a twitch of the velum, and is added to the yolk accumulated at the mouth.
Mentions: For the Encapsulated Experiment 6 capsules were removed from the female and each was placed individually in a Petri dish. Three capsules were assigned to the treatment and 3 were assigned to the control (Figure 1). For treated capsules 20–40% of the embryos within a single capsule were killed by applying pressure to the intact capsule with thin flat forceps (Figure 2). Care was taken not to rupture the capsule wall, and any capsules that appeared damaged were discarded. Observation of the treated capsules showed that the small yolk particles were cleared from the capsule fluid within 2–3 hours and that larger fragments took longer to clear (Figure 2). Because the capsules are a closed system, and because undamaged embryos were observed to capture and ingest yolk particles (Figures 3 & 4, Video S1), it seems likely that this material was ingested. For the control group, the intact capsules were each left in a Petri dish without killing any of the embryos. Broods from 9 females were used for C. cf. marginalis, 11 for C. spinosum, and 16 for B. calyptraeformis.

Bottom Line: We found an overall increase in shell length and velum diameter when embryos feed on damaged siblings within their capsules.The overall effect of our treatment was small compared to the embryonic growth observed in naturally adelphophagic development.These results suggest that the ability to consume, assimilate, and benefit from yolk and tissue of their siblings is widespread across calyptraeids.

View Article: PubMed Central - PubMed

Affiliation: Smithsonian Tropical Research Institute, Balboa, Ancon, Republic of Panama; Universität Oldenburg, Oldenburg, Germany.

ABSTRACT
Adelphophagy, development where embryos grow large by consuming morphologically distinct nutritive embryos or their own normal siblings is widespread but uncommon among animal phyla. Among invertebrates it is particularly common in some families of marine gastropods and segmented worms, but rare or unknown in other closely related families. In calyptraeid gastropods phylogenetic analysis indicates that adelphophagy has arisen at least 9 times from species with planktotrophic larval development. This pattern of frequent parallel evolution of adelphophagy suggests that the embryos of planktotrophic species might be predisposed to evolve adelphophagy. Here we used embryos of three species of planktotrophic calyptraeids, one from each of three major genera in the family (Bostrycapulus, Crucibulum, and Crepidula), to answer the following 3 questions: (1) Can embryos of species with planktotrophic development benefit, in terms of pre-hatching growth, from the ingestion of yolk and tissue from experimentally damaged siblings? (2) Does ingestion of this material from damaged siblings increase variation in pre-hatching size? and (3) Does this experimentally induced adelphophagy alter the allometry between the velum and the shell, increasing morphological similarity to embryos of normally adelphophagic species? We found an overall increase in shell length and velum diameter when embryos feed on damaged siblings within their capsules. There was no detectable increase in variation in shell length or velum diameter, or changes in allometry. The overall effect of our treatment was small compared to the embryonic growth observed in naturally adelphophagic development. However each embryo in our experiment probably consumed less than one sibling on average, whereas natural adelphophages often each consume 10-30 or more siblings. These results suggest that the ability to consume, assimilate, and benefit from yolk and tissue of their siblings is widespread across calyptraeids.

Show MeSH
Related in: MedlinePlus