Multiple paternity and sperm storage in turtles (original) (raw)

Polyandry pays off: The effects of multiple mating and number of fathers on morphological traits and survival in clutches of nesting green turtles at Tortuguero

Despite the long debate of whether or not multiple mating benefits the offspring, studies still show contradicting results. Multiple mating takes time and energy. Thus, if females fertilize their eggs with a single mating, why to mate more than once? We investigated and inferred paternal identity and number of sires in 12 clutches (240 hatchlings) of green turtles (Chelonia mydas) nests at Tortuguero, Costa Rica. Paternal alleles were inferred through comparison of maternal and hatchling genotypes, and indicated multiple paternity in at least 11 of the clutches (92%). The inferred average number of fathers was three (ranging from 1 to 5). This in returns suggests that most females successfully got fecundated by at least three males. Moreover, regression analyses were used to investigate for correlation of inferred clutch paternity with morphological traits of hatchlings fitness (emergence success, length, weight and crawling speed); and size of the mother; and an environmental varia...

Multiple paternity in egg clutches of hawksbill turtles (Eretmochelys imbricata)

Conservation Genetics, 2011

We present the first data collected on the genetic mating system of the hawksbill turtle Eretmochelys imbricata, the only marine turtle not studied to date. We examined paternity within 12 egg clutches from ten female hawksbill turtles from Sabah Turtle Islands, Malaysia. A total of 375 hatchlings were analysed using five microsatellite markers. Results demonstrated that clutches from two out of ten females were sired by multiple males (maximum of two). Although at a low frequency, observation of multiple paternity indicates that hawksbill turtles exhibit the same genetic mating system (polyandry) as observed for other species of marine turtles. Consistent paternity across multiple clutches laid by individual females in one breeding season supports the hypothesis that sperm are stored from mating prior to nesting and are then used to fertilize all subsequent clutches of eggs that season.

Single paternity of clutches and sperm storage in the promiscuous green turtle (Chelonia mydas

Molecular Ecology, 1998

Paternity of 22 green turtle (Chelonia mydas) clutches from 13 females of the southern Great Barrier Reef breeding population was determined through microsatellite analyses at five loci, including the analysis of successive clutches for nine of the females. A large number of alleles per locus (10-40) provided probabilities of detecting multiple paternity that were quite high, particularly at all loci combined (99.9%). Although green turtles are promiscuous breeders and there was an expectation of finding extensive multiple paternity, only two clutches were multiply sired and, in these, very few eggs had been fertilized by a secondary male. The rarity of multiple paternity may reflect either a low proportion of multiple matings by females in this population, or sperm competition, possibly resulting from a first-male sperm preference. Additionally, the analysis of > 900 offspring provided data on mutations, which included 20 mutation events that were observed in 27 offspring and involved both maternal and paternal lineages. Most mutations (n = 16) occurred at a single highly variable locus and their presence emphasizes the need to use multiple loci in paternity studies.

Does polyandry really pay off? The effects of multiple mating and number of fathers on morphological traits and survival in clutches of nesting green turtles at Tortuguero

PeerJ, 2015

Despite the long debate of whether or not multiple mating benefits the offspring, studies still show contradictory results. Multiple mating takes time and energy. Thus, if females fertilize their eggs with a single mating, why to mate more than once? We investigated and inferred paternal identity and number of sires in 12 clutches (240 hatchlings) of green turtles (Chelonia mydas) nests at Tortuguero, Costa Rica. Paternal alleles were inferred through comparison of maternal and hatchling genotypes, and indicated multiple paternity in at least 11 of the clutches (92%). The inferred average number of fathers was three (ranging from 1 to 5). Moreover, regression analyses were used to investigate for correlation of inferred clutch paternity with morphological traits of hatchlings fitness (emergence success, length, weight and crawling speed), the size of the mother, and an environmental variable (incubation temperature). We suggest and propose two different comparative approaches for evaluating morphological traits and clutch paternity, in order to infer greater offspring survival. First, clutches coded by the exact number of fathers and second by the exact paternal contribution (fathers who gives greater proportion of the offspring per nest). We found significant differences (P < 0.05) in clutches coded by the exact number of fathers for all morphological traits. A general tendency of higher values in offspring sired by two to three fathers was observed for the length and weight traits. However, emergence success and crawling speed showed different trends which unable us to reach any further conclusion. The second approach analysing the paternal contribution showed no significant difference (P > 0.05) for any of the traits. We conclude that multiple paternity does not provide any extra benefit in the morphological fitness traits or the survival of the offspring, when analysed following the proposed comparative statistical methods.

Reconstructing paternal genotypes to infer patterns of sperm storage and sexual selection in the hawksbill turtle

Molecular Ecology, 2013

Postcopulatory sperm storage can serve a range of functions, including ensuring fertility, allowing delayed fertilization and facilitating sexual selection. Sperm storage is likely to be particularly important in wide-ranging animals with low population densities, but its prevalence and importance in such taxa, and its role in promoting sexual selection, are poorly known. Here, we use a powerful microsatellite array and paternal genotype reconstruction to assess the prevalence of sperm storage and test sexual selection hypotheses of genetic biases to paternity in one such species, the critically endangered hawksbill turtle, Eretmochelys imbricata. In the majority of females (90.7%, N = 43), all offspring were sired by a single male. In the few cases of multiple paternity (9.3%), two males fertilized each female. Importantly, the identity and proportional fertilization success of males were consistent across all sequential nests laid by individual females over the breeding season (up to five nests over 75 days). No males were identified as having fertilized more than one female, suggesting that a large number of males are available to females. No evidence for biases to paternity based on heterozygosity or relatedness was found. These results indicate that female hawksbill turtles are predominantly monogamous within a season, store sperm for the duration of the nesting season and do not re-mate between nests. Furthermore, females do not appear to be using sperm storage to facilitate sexual selection. Consequently, the primary value of storing sperm in marine turtles may be to uncouple mating and fertilization in time and avoid costly re-mating.

A Review of Patterns of Multiple Paternity Across Sea Turtle Rookeries

Advances in marine biology, 2018

Why females would mate with multiple partners and have multiple fathers for clutches or litters is a long-standing enigma. There is a broad dichotomy in hypotheses ranging from polyandry having benefits to simply being an unavoidable consequence of a high incidence of male-female encounters. If females simply give in to mating when it is too costly to avoid being harassed by males (convenience polyandry), then there should be a higher rate of mating as density increases. However, if females actively seek males because they benefit from multiple mating, then mating frequency, and consequently the incidence of multiple paternity of clutches, should be high throughout. To explore these competing explanations, here we review the incidence of multiple paternity for sea turtles nesting around the World. Across 30 rookeries, including all 7 species of sea turtle, the incidence of multiple paternity was only weakly linked to rookery size (r=0.14). However, using high resolution at-sea GPS t...

First observation of multiple paternity in loggerhead sea turtles, Caretta caretta, nesting on Dalyan Beach, Turkey

Journal of Experimental Marine Biology and Ecology, 2017

Sea turtles are promiscuous breeders with both males and females mating multiply. Due to this mating system, multiple paternity (MP) occurs in sea turtle clutches, and the frequency of MP varies greatly within and among species. In this study, the paternity of a population of loggerhead sea turtles (Caretta caretta) nesting on Dalyan Beach in Turkey was investigated using two highly polymorphic microsatellite markers (CcP2F11 and CcP7C06). Tissue samples collected from randomly selected hatchlings (a total of 522 hatchlings) from two to three successive clutches (a total of 25 clutches) of 10 nesting females were used for paternity analysis with an average sampling effort of 28.2% of offspring per clutch. Evidence of MP in seven out of 10 females (70%) was found, and it was detected that four out of these seven females mated with at least two males, whereas the remaining three females with at least three males. By analysing the successive clutches of females, it was detected that both the number and genotype of contributing sires was same in all clutches of a given female, possibly due to the lack of successful inter-nesting mating in this population. The high frequency of MP implies the possible high genetic diversity within this population. This study indicates that the density of individuals may be the reason of the high frequency of MP in this relatively small population because mating takes place mainly in a narrow area in Dalyan. The possible mating behaviours of the sea turtles and their population structures were discussed in light of the high frequency of MP within this population reported for the first time.

Influences on male reproductive success in long-lived Blanding's Turtles (Emydoidea blandingii)

Canadian Journal of Zoology, 2015

Knowing how the number and qualities of mates influence male reproductive success (RS) can help interpret mating-system dynamics that are important for conservation efforts. We combined parentage data (1999–2006) with data from a long-term life-history study (1953–2007) of Blanding’s Turtles (Emydoidea blandingii (Holbrook, 1838)) on the University of Michigan’s E.S. George Reserve to document the relative influence of mate number and quality on male RS. Blood samples were taken from >92% of resident adults and tissue samples were taken from 723 hatchlings from 92 nests of 54 females over eight nesting seasons. The incidence of multiple paternity averaged 41.6% (N = 77), was variable among years (minimum–maximum = 15.4%–55.6%), and was positively associated with female age, body size, and clutch size. Repeat paternity was observed in 69.9% of sequential clutches of the same female separated by 1–7 years. Male RS was variable (1–40 offspring) and was positively associated with the...

Polyandry in a marine turtle: Females make the best of a bad job

Proceedings of the National Academy of Sciences, 2004

The female perspective on reproductive strategies remains one of the most active areas of debate in biology. Even though a single mating is often sufficient to satisfy the fertilization needs of most females and the act of further mating incurs costs, multiple paternity within broods or clutches is a common observation in nature. Direct or indirect advantage to females is the most popular explanation. However, the ubiquity of this explanation is being challenged by an increasing number of cases for which benefits are not evident. For the first time, we test possible fitness correlates of multiple paternity in a marine turtle, an organism that has long attracted attention in this area of research. Contrary to the wide-spread assumption that multiple mating by female marine turtles confers fitness benefits, none were apparent. In this study, the environment played a far stronger role in determining the success of clutches than whether paternity had been single or multiple. A more like...

Variation in female reproductive quality and reproductive success of male Midland Painted Turtles ( Chrysemys picta marginata )

Canadian Journal of Zoology, 2011

Although mate number is perceived to be the primary factor affecting male reproductive success in polygynous systems, differences in female reproductive qualities may also influence variation in male reproductive success. We combined 32 years of data on variation in reproductive qualities (clutch size and clutch frequency) of female Midland Painted Turtles (Chrysemys picta marginata Agassiz, 1857) with genetic data on patterns of repeated paternity (i.e., stored sperm use) and multiple paternity to examine the potential influence on male reproductive success. Over 24 years , the number of reproductive females each year averaged 84 (minimum-maximum = 62-106) and, on average, 23% (minimum-maximum = 6%-40%) produced two clutches (intraseasonally). Among females with reproductive histories spanning 5-24 years (N = 167), 26% of individuals produced only one clutch annually, whereas 74% produced two clutches within a season. Among just intraseasonally iteroparous females, second-clutch production varied from 7% to 50%. Repeated paternity was observed in 97.5% of 40 paired clutches and 44% of 9 among-year comparisons of clutches from consecutive years. The frequent use of stored sperm to fertilize sequential clutches within and potentially among years can substantially increase a male's reproductive success, particularly if males can base mating decisions on phenotypic characteristics correlated with female quality.