Is multiple paternity in elasmobranchs a plesiomorphic characteristic?

Lamarca, Felipe; Carvalho, Pedro Hollanda; Vilasboa, Anderson; Netto‐Ferreira, André L.; Viana, Marcelo Machado

doi:10.1007/s10641-020-01034-y

Cited by 12 publications

(21 citation statements)

References 31 publications

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“…Our study provides a comprehensive analysis and novel approach for considering the drivers of multiple paternity in elasmobranchs. While it is becoming clear that polyandry is more the rule than the exception (Lamarca et al, 2020), the exact mechanisms behind this phenomenon have received little attention beyond the notion of convenience polyandry, which is difficult to empirically demonstrate (Boulton et al, 2018) and has not been formally tested in elasmobranchs. While we do not discount male‐based drivers as playing an important role in the reproductive process, we caution against these being used as the only explanations for the high occurrence of polyandry across elasmobranch mating systems in the absence of empirical testing.…”

Section: Discussionmentioning

confidence: 99%

“…In the absence of mate choice, females may lower their fitness risk by increasing the number of sires, which would result in an increase in polyandry. Indeed, the occurrence of multiple paternity across elasmobranch species is widespread (Lamarca et al, 2020), with nearly every species examined exhibiting some degree of multiple paternity (Table 1). Explanations of this phenomenon are most often casually attributed to “convenience polyandry,” where females are presumed to mate with multiple males simply because the cost of avoiding rigorous copulatory behaviour is too high (e.gBarker et al, 2019; DiBattista et al, 2008; DiBattista et al, 2008; Feldheim et al, 2004; Griffiths et al, 2011; Lage et al, 2008; Nosal et al, 2013; Pirog et al, 2017; Rossouw et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

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An inconvenient tooth: Evaluating female choice in multiple paternity using an evolutionarily and ecologically important vertebrate clade

2021

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Understanding mating systems is a pillar of behavioural ecology, placing the complex interactions between females and males into a reproductive context. The field of multiple paternity, the phenomenon whereby many sires contribute to an individual litter, has traditionally viewed females as passive players in a male–male competitive framework. With the emergence of feminist perspectives in ecological fields, novel alternative mechanisms and evolutionary theories across invertebrate and vertebrate taxa recognize females are active stakeholders in the reproductive process. Despite their evolutionary significance, ecological diversity and myriad reproductive modes, elasmobranch (sharks, skates and rays) research lags behind other fields regarding complex biological processes, such as multiple paternity which is often ascribed to convenience polyandry. Here, we layout hypotheses and resynthesize multiple paternity literature from a female and life history perspective to highlight how alternative mechanisms influence the predominance of multiple paternity across elasmobranchs. We draw upon parallels in other invertebrate and vertebrate taxa to demonstrate how female elasmobranchs can influence multiple paternity outcomes that benefit their reproductive success. Our article challenges dogma that has resulted from years of dismissing the female perspective as important and provides a framework for future advancement using more holistic approaches to studying mating systems.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

An inconvenient tooth: Evaluating female choice in multiple paternity using an evolutionarily and ecologically important vertebrate clade

2021

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“…When female sharks copulate with more than one male over the breeding season (polyandry), a common strategy in elasmobranchs (Fitzpatrick et al, 2012), the first male to mate can sire the majority of the litter (Orr and Brennan, 2015). This reproductive skew should increase male competition to access females early in their reproductive cycle (Bateman, 1948), but polyandry appears rare or absent in tiger sharks: studies on Indian and Pacific Ocean populations indicate that tiger sharks may be one of a relatively few species to utilize genetic monogamy (Holmes et al, 2018;Pirog et al, 2020), especially over multiple cycles (Lamarca et al, 2020). In practice, a limit on receptive females would increase the selective pressure on male tiger sharks to be the first to encounter such individuals, promoting the evolution of reproductive site fidelity.…”

Section: Discussionmentioning

confidence: 99%

Age-Dependent Dispersal and Relatedness in Tiger Sharks (Galeocerdo cuvier)

et al. 2022

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Understanding dispersal in large marine fauna is necessary for conservation, but movement patterns often vary widely by sex and life stage. In sharks, genetic studies have shown evidence of widespread male-biased dispersal, though tagging and tracking studies on the same populations show both sexes using site fidelity, including philopatry, and moving similar distances. We used a suite of microsatellite loci and DNA samples from 362 previously-tagged tiger sharks (Galeocerdo cuvier) in the northwestern Atlantic, including a large number of residential juveniles, to evaluate reproductive dispersal in light of demographic and published tracking data. We found that lumping size classes together resulted in genetic panmixia across sites, but systematic removal of large individuals showed significant population-level differentiation and three separate population clusters among juveniles less than 260 cm total length. Tests for relatedness found that 8.9% of our sample set was composed of first-order related pairs (N = 16), including several full siblings from different litters, a sign of multi-cycle genetic monogamy which carries implications for effective population size. By mapping genetic assignments of juveniles, we identified a signature of fine-scale genetic structure suggesting broad biparental site fidelity to reproductive habitat in the northeast Gulf of Mexico, which is concordant with both genetic and tracking data. Taken together, these findings demonstrate how lumping individuals from different life stages in genetic studies may obscure fine-scale genetic structure, confounding future conservation efforts.

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“…MP has been an important topic for research in the Elasmobranchii, which includes sharks and rays (Lyons et al ., 2021). To date, MP is reported for 35 elasmobranchs (Lamarca et al ., 2020a); only three of them being rays (Batoidea), two myliobatiform species (Janse et al ., 2013; Lyons et al ., 2017) and one rajiform species (Chevolot et al ., 2007). This unbalanced number of studies on MP for sharks and rays does not reflect the fact that the Batoidea is more specious than the Selachii (Last et al ., 2016).…”

Section: Loci Pleo83 Pleo120 Pleo187mentioning

confidence: 99%

“…The present study is the first report of MP in Potamotrygonidae and the fourth in the Batoidea. MP was observed in Urobatis helleri , a species of Urotrygonidae (Lyons et al ., 2017), which is considered a closely related clade to Potamotrygonidae (Last et al ., 2016), therefore supporting the previous findings of the widespread presence of MP in elasmobranchs (Lamarca et al ., 2020a). Considering this, the detection of MP in P. leopoldi points to the likely occurrence of MP in other neotropical freshwater stingrays.…”

Section: Loci Pleo83 Pleo120 Pleo187mentioning

confidence: 99%

Evidence of multiple paternity for the endemic Xingu River stingray

Torres

Charvet

Faria

et al. 2022

Journal of Fish Biology

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Multiple paternity (MP) is a phenomenon observed for more than 30 elasmobranch species. The Batoidea is more specious than the Selachii, but only three studies of MP have been conducted on batoids. The occurrence of MP in freshwater stingrays was tested using microsatellite markers, which were developed for Potamotrygon leopoldi. Six mothers and their litters were genotyped, providing the first evidence of MP for Potamotrygonidae, with an MP frequency of 33%.

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Is multiple paternity in elasmobranchs a plesiomorphic characteristic?

Cited by 12 publications

References 31 publications

An inconvenient tooth: Evaluating female choice in multiple paternity using an evolutionarily and ecologically important vertebrate clade

An inconvenient tooth: Evaluating female choice in multiple paternity using an evolutionarily and ecologically important vertebrate clade

Age-Dependent Dispersal and Relatedness in Tiger Sharks (Galeocerdo cuvier)

Evidence of multiple paternity for the endemic Xingu River stingray

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