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Mechanosensory feedback of the internal reproductive state drives decisions about when and where to reproduce. For instance, stretch in the Drosophila reproductive tract produced by artificial distention or from accumulated eggs regulates the attraction to acetic acid to ensure optimal oviposition. How such mechanosensory feedback modulates neural circuits to coordinate reproductive behaviors is incompletely understood. We previously identified a stretch-dependent homeostat that regulates egg laying in Caenorhabditis elegans. Sterilized animals lacking eggs show reduced Ca2+ transient activity in the presynaptic HSN command motoneurons that drive egg-laying behavior, while animals forced to accumulate extra eggs show dramatically increased circuit activity that restores egg laying. Interestingly, genetic ablation or electrical silencing of the HSNs delays, but does not abolish, the onset of egg laying, with animals recovering vulval muscle Ca2+ transient activity upon egg accumulation. Using an acute gonad microinjection technique to mimic changes in pressure and stretch resulting from germline activity and egg accumulation, we find that injection rapidly stimulates Ca2+ activity in both neurons and muscles of the egg-laying circuit. Injection-induced vulval muscle Ca2+ activity requires L-type Ca2+ channels but is independent of presynaptic input. Conversely, injection-induced neural activity is disrupted in mutants lacking the vulval muscles, suggesting "bottom-up" feedback from muscles to neurons. Direct mechanical prodding activates the vulval muscles, suggesting that they are the proximal targets of the stretch-dependent stimulus. Our results show that egg-laying behavior in C. elegans is regulated by a stretch-dependent homeostat that scales postsynaptic muscle responses with egg accumulation in the uterus.
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TREE HOLES TO TRASH: UNIQUE UPSIDE-DOWN TERRESTRIAL SPAWNING, AGONISTIC INTERACTIONS, COMPLEX MATING CALLS, AND UNNATURAL BREEDING ALTERATIONS IN MINERVARYA CHARLESDARWINI (ANURA, DICROGLOSSIDAE)
Anuran amphibians exhibit the greatest diversity of reproductive modes among tetrapod vertebrates. The Andamanese Charles Darwin's frog, Minervarya charlesdarwini, is the only species of the family Dicroglossidae that is known to naturally deposit eggs in water-filled cavities of tree holes or buttresses, where they then undergo exotrophic development. We describe the reproductive behavior in this species that involves a unique combination of traits: (1) Males produce complex advertisement calls comprising at least three different call types, in addition to a type of aggressive call. (2) Unpaired males exhibit agonistic interactions with each other and with mated pairs. (3) Mate selection, amplexus, and oviposition take place inside water-filled cavities. (4) During axillary amplexus, mating pairs synchronously switch between head-up and head-down positions above and below the water surface using both forward and backward movements. (5) At the time of egg laying, amplectant pairs are in an upside-down position on the cavity walls with their bodies completely outside the water. (6) Eggs are deposited over multiple bouts on the inner walls of the cavities and terrestrially above the water surface. Upside-down spawning in M. charlesdarwini is a unique trait among phytotelm-breeding terrestrial frogs. The combination of terrestrial oviposition sites in water-filled phytotelmata and the upside-down egg-laying posture is a novel report for the family Dicroglossidae and perhaps all anurans. This specialized behavior is also likely derived for a species that is embedded in a group of largely aquatic-breeding minervaryan frogs. Although M. charlesdarwini appears to be an obligate phytotelm breeder, individuals were often observed breeding inside cylindrical, water-filled plastic sapling bags in plant nurseries adjacent to fragmented forest patches, or in rain-filled discarded plastic, glass, or metal containers left as trash at the forest edge. Use of such unnatural breeding sites is likely a forced behavioral shift in response to rapidly changing forest landscapes associated with recent habitat loss and fragmentation. Our findings call for conservation attention to this habitat specialist, which, although locally abundant, is an endemic and threatened species of the Andaman Islands.
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- Award ID(s):
- 2122620
- PAR ID:
- 10630012
- Publisher / Repository:
- Museum of Comparative Zoology, Harvard University
- Date Published:
- Journal Name:
- Breviora
- Volume:
- 577
- ISSN:
- 0006-9698
- Page Range / eLocation ID:
- 1-33
- Subject(s) / Keyword(s):
- Amphibia Andaman and Nicobar Islands frog behavior amplexus bioacoustics conservation oviposition phytotelm breeding reproductive mode
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.3099/0006-9698-577.1.1
