Exceptional long-term sperm storage by a female vertebrate

Abstract

Females of many vertebrate species have the capacity to store sperm within their reproductive tracts for prolonged periods of time. Termed long-term sperm storage, this phenomenon has many important physiological, ecological, and evolutionary implications, particularly to the study of mating systems, including male reproductive success and post-copulatory sexual selection. Reptiles appear particularly predisposed to long-term sperm storage, with records in most major lineages, with a strong emphasis on turtles and squamates (lizards, snakes, but not the amphisbaenians). Because facultative parthenogenesis is a competing hypothesis to explain the production of offspring after prolonged separation from males, the identification of paternal alleles through genetic analysis is essential. However, few studies in snakes have undertaken this. Here, we report on a wild-collected female Western Diamond-backed Rattlesnake, Crotalus atrox, maintained in isolation from the time of capture in September 1999, that produced two healthy litters approximately one and six years post capture. Genetic analysis of the 2005 litter, identified paternal contribution in all offspring, thus rejecting facultative parthenogenesis. We conclude that the duration of long-term sperm storage was approximately 6 years (71 months), making this the longest period over which a female vertebrate has been shown to store sperm that resulted in the production of healthy offspring.

The life history of Drosophila sperm involves molecular continuity between male and female reproductive tracts

“…Sperm are streamlined cells with a limited capacity for transcription, so their survival and fertilization success depend on support and protection during the period between ejaculation and fertilization ( 25 ). This is particularly important in species with long periods of sperm storage in the FRT, as occurs in diverse invertebrate and vertebrate taxa ( 8 , 25 , 26 ). Carbohydrates and proteins from seminal fluid support energy production and enhance viability during ejaculation and immediately after sperm transfer ( 27 – 29 ), but most seminal components do not persist throughout the duration of sperm storage ( 25 ).…”

Biotecnologias reprodutivas em serpentes: uma análise cieniométrica

“…Another factor that may corroborate the understanding of this high sperm concentration is the reproductive potential of the females of these animals in maintaining the viability of male gametes in their organism for a high and still unknown time (Levine et al, 2021). Thus, fertilization can occur at different reproductive periods, as demonstrated in the study by Levine et al (2021), in which females of Crotalus atrox (Baird; Girard, 1853) maintained viable sperm for six years after copulation, generating diploid pups, genetically corresponding to the male with whom they had the last sexual interaction.…”

Parentage assignment reveals multiple paternity in the critically-endangered Guatemalan beaded lizard (Heloderma charlesbogerti)

“…While females were observed to exhibit serial polyandry, females were also found to produce offspring with the same male across seasons, either in single-or multiple-paternity clutches. It was not possible here to determine whether these resulted from long-term sperm storage (LTSS) across seasons, however LTSS has been reported in other reptiles, with the production of viable offspring resulting from the storage of sperm for up to six years (Booth & Schuett, 2011;Levine et al 2021). Observations at Zoo Atlanta of eggs laid by females that had been with males in previous seasons but not housed with males in following seasons have not provided evidence of LTSS as in all cases eggs failed to show signs of development.…”