High Levels of Multiple Paternity in Littorina saxatilis: Hedging the Bets?

Mäkinen, Tuuli; Panova, Marina; André, Carl

doi:10.1093/jhered/esm097

Cited by 42 publications

(52 citation statements)

References 55 publications

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“…For this, simulation analyses implemented in the software PrDM [43] were run for scenarios of equal, moderately skewed, and highly skewed paternal contribution taking into account a varying number (two to ten) of participant males in a brood. This range of participant males is in accordance with the level of multiple paternity observed in other aquatic gastropods [44,45]. …”

Section: Methodssupporting

confidence: 88%

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Paternity Outcomes in the Freshwater Gastropod, Chilina dombeiana in the Biobío River, Chile

Bórquez

Brante

2017

PLoS ONE

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Studying the mating system of obligate aquatic organisms that inhabit river ecosystems is important for understanding its evolution as well as the role of biological and environmental factors in modulating population dynamics and species distributional patterns. Here, we studied the reproductive strategy of the Chilean endemic freshwater snail, Chilina dombeiana, in the Biobío River, one of the largest rivers in Chile. This species has a low potential for dispersal given the absence of a free-swimming larval stage (benthic larval development) and given that adults have a low capacity for mobility. We hypothesized that: 1. Females would mate with different males (polyandry) resulting in intrabrood multiple paternity, 2. Individuals from closer sites would be more related than individuals from distant sites, and 3. Male parental contributions would be unevenly distributed within broods. Individuals from three different sites were sampled along the river: upper, mid, and river mouth. In the laboratory, hatching juveniles from a total of 15 broods were collected for paternity analyses. We used microsatellite markers and the programs GERUD and COLONY to determine whether multiple paternity exists and to estimate the contribution of different males to the brood. We found that multiple paternity was very common at all of the sites analyzed with as many as 8 males fertilizing a single female and a mean of 4.2 fathers per brood estimated by COLONY. Sire contribution was skewed to particular males in several broods. In addition, overall relatedness among broods for the three sites ranged from 0.17 to 0.45 with evidence of many half-siblings. Relatedness differed among the three sites. Particularly in upstream sites or in anthropogenically disturbed populations, the high levels of multiple paternity observed in C. dombeiana may be an efficient strategy to avoid inbreeding and prevent the loss of genetic diversity within populations.

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Section: Methodssupporting

confidence: 88%

“…marine species: [61,45,3,4,5]; freshwater species: [23]). Several decades ago, studies using enzyme electrophoresis reported multiple paternity in freshwater pulmonates such as Biomphalaria obstructa [62], Bulinus africanus [63], B .…”

Section: Discussionmentioning

confidence: 99%

Paternity Outcomes in the Freshwater Gastropod, Chilina dombeiana in the Biobío River, Chile

Bórquez

Brante

2017

PLoS ONE

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“…In an earlier attempt to estimate the level of multiple paternity in L. saxatilis we detected an average of 7.6 males contributing to broods of wild-mated females [24]. However, we analysed only 20–23 out of 23 to 87 offspring per brood.…”

Section: Introductionmentioning

confidence: 99%

Extreme Female Promiscuity in a Non-Social Invertebrate Species

et al. 2010

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BackgroundWhile males usually benefit from as many matings as possible, females often evolve various methods of resistance to matings. The prevalent explanation for this is that the cost of additional matings exceeds the benefits of receiving sperm from a large number of males. Here we demonstrate, however, a strongly deviating pattern of polyandry.Methodology/Principal FindingsWe analysed paternity in the marine snail Littorina saxatilis by genotyping large clutches (53–79) of offspring from four females sampled in their natural habitats. We found evidence of extreme promiscuity with 15–23 males having sired the offspring of each female within the same mating period.Conclusions/SignificanceSuch a high level of promiscuity has previously only been observed in a few species of social insects. We argue that genetic bet-hedging (as has been suggested earlier) is unlikely to explain such extreme polyandry. Instead we propose that these high levels are examples of convenience polyandry: females accept high numbers of matings if costs of refusing males are higher than costs of accepting superfluous matings.

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“…), multiply-fertilized individuals accounted for about 76%–100% among all of the studied females, and the number of sires per brood ranged from 1–23. Patterns of sperm competition are variable in these species, some have no male sperm precedence [18], [22], [23] whilst others have last male sperm precedence [16], [19].…”

Section: Introductionmentioning

confidence: 99%

Microsatellite Evidence for High Frequency of Multiple Paternity in the Marine Gastropod Rapana venosa

2014

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BackgroundInferring of parentage in natural populations is important in understanding the mating systems of a species, which have great effects on its genetic structure and evolution. Muricidae, a large group (approximately 1,600 species) of marine gastropods, are poorly investigated in patterns of multiple paternity and sperm competition based on molecular techniques. The veined Rapa whelk, Rapana venosa, a commercially important muricid species with internal fertilization, is an ideal species to study the occurrence and frequency of multiple paternity and to facilitate understanding of their reproductive strategies.Methodology/Principal FindingsWe developed five highly polymorphic microsatellites in R. venosa and applied them to identify multiple paternity in 19 broods (1381 embryos) collected from Dandong, China. Multiple paternity was detected in 17 (89.5%) of 19 broods. The number of sires per brood ranged from 1 to 7 (4.3 on average). Of the 17 multiply sired broods, 16 (94.1%) were significantly skewed from equal paternal contributions, and had a dominant sire which was also dominant in each assayed capsule.ConclusionsOur results indicate that a high level of multiple paternity occurs in the wild population of R. venosa. Similar patterns of multiple paternity in the 2–6 assayed capsules from each brood imply that fertilization events within the body of a female occur mostly (but not entirely) as random draws from a “well-but-not-perfectly blended sperm pool” of her several mates. Strongly skewed distributions of fertilization success among sires also suggest that sperm competition and/or cryptic female choice might be important for post-copulatory paternity biasing in this species.

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High Levels of Multiple Paternity in Littorina saxatilis: Hedging the Bets?

Cited by 42 publications

References 55 publications

Paternity Outcomes in the Freshwater Gastropod, Chilina dombeiana in the Biobío River, Chile

Paternity Outcomes in the Freshwater Gastropod, Chilina dombeiana in the Biobío River, Chile

Extreme Female Promiscuity in a Non-Social Invertebrate Species

Microsatellite Evidence for High Frequency of Multiple Paternity in the Marine Gastropod Rapana venosa

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