Dataset Information

Unique reproductive strategy in the swamp wallaby.

ABSTRACT: Reproduction in mammals requires distinct cycles of ovulation, fertilization, pregnancy, and lactation often interspersed with periods of anoestrus when breeding does not occur. Macropodids, the largest extant species of marsupials, the kangaroos and wallabies, have a very different reproductive strategy to most eutherian mammals whereby young are born at a highly altricial stage of development with the majority of development occurring over a lengthy lactation period. Furthermore, the timings of ovulation and birth in some species occurs within a very short interval of each other (sometimes hours). Female swamp wallabies have an oestrous cycle shorter than their pregnancy length and were, therefore, speculated to mate and form a new embryo before birth thereby supporting two conceptuses at different stages of pregnancy. To confirm this, we used high-resolution ultrasound to monitor reproduction in swamp wallabies during pregnancy. Here, we show that females ovulate, mate, and form a new embryo prepartum while still carrying a full-term fetus in the contralateral uterus. This embryo enters embryonic diapause until the newborn leaves the pouch 9 mo later. Thus, combined with embryonic diapause, females are continuously pregnant and lactating at the same time throughout their reproductive life, a unique reproductive strategy that completely blurs the normal staged system of reproduction in mammals.

SUBMITTER: Menzies BR

PROVIDER: S-EPMC7084135 | biostudies-literature | 2020 Mar

REPOSITORIES: biostudies-literature

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Unique reproductive strategy in the swamp wallaby.

Menzies Brandon R BR Hildebrandt Thomas B TB Renfree Marilyn B MB

Proceedings of the National Academy of Sciences of the United States of America 20200302 11

Reproduction in mammals requires distinct cycles of ovulation, fertilization, pregnancy, and lactation often interspersed with periods of anoestrus when breeding does not occur. Macropodids, the largest extant species of marsupials, the kangaroos and wallabies, have a very different reproductive strategy to most eutherian mammals whereby young are born at a highly altricial stage of development with the majority of development occurring over a lengthy lactation period. Furthermore, the timings o ...[more]

PMID: 32123078

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Project description:BACKGROUND: Small RNAs have proven to be essential regulatory molecules encoded within eukaryotic genomes. These short RNAs participate in a diverse array of cellular processes including gene regulation, chromatin dynamics and genome defense. The tammar wallaby, a marsupial mammal, is a powerful comparative model for studying the evolution of regulatory networks. As part of the genome sequencing initiative for the tammar, we have explored the evolution of each of the major classes of mammalian small RNAs in an Australian marsupial for the first time, including the first genome-scale analysis of the newest class of small RNAs, centromere repeat associated short interacting RNAs (crasiRNAs). RESULTS: Using next generation sequencing, we have characterized the major classes of small RNAs, micro (mi) RNAs, piwi interacting (pi) RNAs, and the centromere repeat associated short interacting (crasi) RNAs in the tammar. We examined each of these small RNA classes with respect to the newly assembled tammar wallaby genome for gene and repeat features, salient features that define their canonical sequences, and the constitution of both highly conserved and species-specific members. Using a combination of miRNA hairpin predictions and co-mapping with miRBase entries, we identified a highly conserved cluster of miRNA genes on the X chromosome in the tammar and a total of 94 other predicted miRNA producing genes. Mapping all miRNAs to the tammar genome and comparing target genes among tammar, mouse and human, we identified 163 conserved target genes. An additional nine genes were identified in tammar that do not have an orthologous miRNA target in human and likely represent novel miRNA-regulated genes in the tammar. A survey of the tammar gonadal piRNAs shows that these small RNAs are enriched in retroelements and carry members from both marsupial and tammar-specific repeat classes. Lastly, this study includes the first in-depth analyses of the newly discovered crasiRNAs. These small RNAs are derived largely from centromere-enriched retroelements, including a novel SINE. CONCLUSIONS: This study encompasses the first analyses of the major classes of small RNAs for the newly completed tammar genome, validates preliminary annotations using deep sequencing and computational approaches, and provides a foundation for future work on tammar-specific as well as conserved, but previously unknown small RNA progenitors and targets identified herein. The characterization of new miRNA target genes and a unique profile for crasiRNAs has allowed for insight into multiple RNA mediated processes in the tammar, including gene regulation, species incompatibilities, centromere and chromosome function.

Project description:Spatiotemporal segregation is often explained by the risk for offspring predation or by differences in physiology, predation risk vulnerability or competitive abilities related to size dimorphism. Most large carnivores are size dimorphic and offspring predation is often intraspecific and related to nonparental infanticide (NPI). NPI can be a foraging strategy, a strategy to reduce competition, or a male reproductive strategy. Spatiotemporal segregation is widespread among large carnivores, but its nature remains poorly understood. We evaluated three hypotheses to explain spatiotemporal segregation in the brown bear, a size-dimorphic large carnivore in which NPI is common; the 'NPI - foraging/competition hypothesis', i.e. NPI as a foraging strategy or a strategy to reduce competition, the 'NPI - sexual selection hypothesis', i.e. infanticide as a male reproductive strategy and the 'body size hypothesis', i.e. body-size-related differences in physiology, predation risk vulnerability or competitive ability causes spatiotemporal segregation. To test these hypotheses, we quantified spatiotemporal segregation among adult males, lone adult females and females with cubs-of-the-year, based on GPS-relocation data (2006-2010) and resource selection functions in a Scandinavian population. We found that spatiotemporal segregation was strongest between females with cubs-of-the-year and adult males during the mating season. During the mating season, females with cubs-of-the-year selected their resources, in contrast to adult males, in less rugged landscapes in relative close proximity to certain human-related variables, and in more open habitat types. After the mating season, females with cubs-of-the-year markedly shifted their resource selection towards a pattern more similar to that of their conspecifics. No strong spatiotemporal segregation was apparent between females with cubs-of-the-year and conspecifics during the mating and the postmating season. The 'NPI - sexual selection hypothesis' best explained spatiotemporal segregation in our study system. We suggest that females with cubs-of-the-year alter their resource selection to avoid infanticidal males. In species exhibiting NPI as a male reproductive strategy, female avoidance of infanticidal males is probably more common than observed or reported, and may come with a fitness cost if females trade safety for optimal resources.

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Dataset Information

Unique reproductive strategy in the swamp wallaby.

Publications

Unique reproductive strategy in the swamp wallaby.

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