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Extreme fertilization bias towards freshly inseminated sperm in a species exhibiting prolonged female sperm storage.

ABSTRACT: The storage of sperm by females across successive reproductive cycles is well documented in internal fertilizers, yet the fate of stored sperm when they compete with 'new' sperm to fertilize a female's eggs has rarely been considered. This gap in our understanding is likely due to the logistical difficulties of controlling behavioural interactions during or after mating, which in turn may influence how many sperm are inseminated and how stored sperm are ultimately used during successive bouts of sperm competition with freshly inseminated sperm. Here, we use artificial insemination (AI) in guppies (Poecilia reticulata), a polyandrous live-bearing poeciliid fish exhibiting prolonged sperm storage by females, to overcome these challenges. The use of AI enables us to control potential differential maternal effects (e.g. behaviourally mediated cryptic female choice) and specifically test for post-copulatory paternity biases that favour either stored or fresh sperm when they compete to fertilize eggs. Our paternity analyses revealed the almost complete dominance of freshly inseminated sperm over stored sperm, supporting previous studies reporting similar patterns following natural matings across successive brood cycles. However, our use of AI, which excluded behavioural interactions between males and females, most likely generated a far stronger pattern of fresh sperm precedence compared with those reported in previous studies, possibly implicating 'cryptic' forms of selection by females that may sometimes bolster the success of stored sperm.

SUBMITTER: Gasparini C

PROVIDER: S-EPMC5882737 | biostudies-literature | 2018 Mar

REPOSITORIES: biostudies-literature

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Extreme fertilization bias towards freshly inseminated sperm in a species exhibiting prolonged female sperm storage.

Gasparini Clelia C Daymond Emma E Evans Jonathan P JP

Royal Society open science 20180307 3

The storage of sperm by females across successive reproductive cycles is well documented in internal fertilizers, yet the fate of stored sperm when they compete with 'new' sperm to fertilize a female's eggs has rarely been considered. This gap in our understanding is likely due to the logistical difficulties of controlling behavioural interactions during or after mating, which in turn may influence how many sperm are inseminated and how stored sperm are ultimately used during successive bouts of ...[more]

PMID: 29657813

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Project description:BackgroundFemale sperm storage (FSS), the maintenance of sperm inside the female reproductive tract for an extended period of time, is pervasive among organisms with internal fertilization. Because FSS enables asynchronous mating and fertilization, it could be extremely important to reproduction. However, the physiological mechanisms underlying prolonged preservation and maintenance are poorly understood. Here, we used chicken, a typical oviparous animal, to determine the mechanisms ensuring sperm functionality in sperm storage tubules (SSTs).ResultsWe performed an insemination experiment on over two thousand hens at two periods, and found that the FSS capabilities varied widely among individuals. Except for the differences in the SST density between the two groups with distinct FSS abilities, we quantitatively profiled small-molecule metabolites derived from SST cells, and identified 28 metabolites with differential expression. In particular, high levels of lipids, fatty acids and lipid peroxidation product were observed in hens with low FSS capability. Pathway analysis showed that these differential metabolites were significantly enriched in the biosynthesis of unsaturated fatty acids. Moreover, we detected the total antioxidant capacity and lipid peroxidation level of SSTs, and found that chickens with a lower FSS ability had a significantly higher content of lipid peroxidation end-product, which was 2.4-fold greater than chickens with a higher FSS capability, and no significant difference was found in the total antioxidant capacity between these two groups.ConclusionsOur findings reveal that the long-term storage of sperm and the maintenance of their function in the female reproductive tract require an adequate microenvironment. The superabundance of fatty acids secreted by SST cells had detrimental effects on sperm storage in the female reproductive tract. Lipid peroxidation produces toxic biological substances that may cause irreversible damage to resident spermatozoa, resulting in short-term sperm retention and decreased fertility. Our findings provide new avenues for studying sperm storage and sustaining fertility.

Dataset Information

Extreme fertilization bias towards freshly inseminated sperm in a species exhibiting prolonged female sperm storage.

Publications

Extreme fertilization bias towards freshly inseminated sperm in a species exhibiting prolonged female sperm storage.

Similar Datasets

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