Is multiple mating beneficial or unavoidable? Low multiple paternity and genetic diversity in the shortspine spurdog Squalus mitsukurii

Abstract

Proposed benefits of multiple paternity include increased reproductive output, elevated fitness of progeny, and maintenance of population genetic diversity. However, another consideration is whether multiple paternity is simply an unavoidable byproduct of sexual conflict, with males seeking to maximize mating encounters while females seek to minimize the stress of copulation. Here we examined the polyandrous mating system in sharks, with a focus on the reproductive genetics of the shortspine spurdog Squalus mitsukurii. Members of the genus Squalus are long-lived, slow-growing, and employ among the longest gestation periods of any vertebrate. To evaluate multiple paternity and genetic diversity in S. mitsukurii, we genotyped 27 litters plus 96 individuals with 8 microsatellite loci. Further, 670 bp of the mtDNA control region were sequenced in 112 individuals to examine population structure. S. mitsukurii in Hawaii showed low genetic diversity relative to other sharks (π = 0.0010 ± 0.0008) and no significant population structure in the Hawaiian Archipelago. Direct allele counts and Bayesian approximations returned concordant estimates of 11% multiple paternity, the lowest observed in sharks to date. Considering the protracted reproductive interval of S. mitsukurii, sexual conflict that results from differential male and female reproductive strategies may favor the development of female mating avoidance behavior to minimize trauma. In S. mitsukurii this behavior includes segregation of sexes and an asynchronous reproductive cycle.KEY WORDS: Elasmobranch · Polyandry · Control region · Microsatellite DNA · Population structure · Sexual conflict · Sexual segregation · Reproductive strategy Resale or republication not permitted without written consent of the publisherMar Ecol Prog Ser 403: [255][256][257][258][259][260][261][262][263][264][265][266][267] 2010 females with conventional sex roles (reviewed by Zeh & Zeh 2003). Polyandry (females mating with more than one male) and multiple paternity (a single brood of offspring sired by multiple males) are now recognized as common strategies in widely divergent taxa including amphibians, mammals, reptiles, insects, crustaceans, and fishes (Evans & Magurran 2000, Toonen 2004, Adams et al. 2005, Bretman & Tregenza 2005, Daly-Engel et al. 2006, Dean et al. 2006, Jensen et al. 2006. It is still unclear, however, what roles sexual conflict and intersexual selection might play in polyandrous mating systems.For males, the advantages to having multiple breeding partners are clear: the more females a male inseminates, the more offspring he fathers and the greater his reproductive fitness. The benefits of polyandry to females are less obvious. Potential direct benefits to the female include nuptial gifts or parental care on the part of the male. No direct benefits have been shown in shark mating systems, though there is potential for indirect or genetic benefits through polyandrous mating. If there is little or no opportunity to evaluate males prior to copulation, a f...

Genetic mating system of the brown smoothhound shark (Mustelus henlei), including a literature review of multiple paternity in other elasmobranch species

“…Here, we used the program PrDM (NeV and Pitcher 2002) to run a number of simulations to test the power aVorded by our suite of microsatellite markers to unveil multiple paternity under several diVerent hypothetical scenarios. Previous research on sharks has detected a range of 1-4 sires per brood (Saville et al 2002;Chapman et al 2004;Feldheim et al 2004;Daly-Engel et al 2006;Portnoy et al 2007;DiBattista et al 2008b;Lage et al 2008;Daly-Engel et al 2010), so here we assume a conservative range of 2-5 sires under equal, as well as skewed, reproductive success. Each simulation was run with litter sizes ranging from 4 to 17 (the minimum and maximum clutch sizes observed in the present study).…”

Relatedness and polyandry of sixgill sharks, Hexanchus griseus, in an urban estuary

“…Multiple paternity obviously results in increased diversity within a litter but, due to variance in reproductive success among males noted in many shark species, increased diversity is not likely seen at the population level (Karl 2008;Daly-Engel et al 2010). In fact, Daly-Engel et al (2010) compared published estimates of percent multiple paternity and genetic diversity within shark species and found no significant correlation.…”

“…Polyandry (females mating with more than one male), polygyny (males mating with more than one female), and multiple paternity within a litter is recognized in many shark species (Feldheim et al 2002;Portnoy et al 2007;DiBattista et al 2008;Daly-Engel et al 2007. Multiple paternity obviously results in increased diversity within a litter but, due to variance in reproductive success among males noted in many shark species, increased diversity is not likely seen at the population level (Karl 2008;Daly-Engel et al 2010). In fact, Daly-Engel et al (2010) compared published estimates of percent multiple paternity and genetic diversity within shark species and found no significant correlation.…”

“…There are few in-depth genetic diversity studies using microsatellite neutral nuclear markers in large shark species. Those that exist report low to moderate genetic diversity in the form of expected heterozygosity; H E : range of 0.12-0.95 for blacktip reef sharks, Carcharhinus limbatus (Keeney et al 2005); 0.23-0.53 for sandbar sharks, Carcharhinus plumbeus (Heist and Gold 1999); 0.61-0.97 for lemon sharks, Negaprion brevirostris (Feldheim et al 2001;Portnoy et al 2007); 0.17-0.90 for nurse sharks, Ginglymostoma cirratum (Heist et al 2003); 0.45-0.95 for great white sharks, Carcharodon carcharias (Pardini et al 2000); 0.47-0.81 for grey nurse shark, Carcharias Taurus (Ahonen et al 2009); 0.40-1.00 for whale shark, Rhincodon typus (Schmidt et al 2009);and 0.35-0.86 for the shortspine spurdog, Squalus mitsukurii (Daly-Engel et al 2010). Using mtDNA, Hoelzel et al (2006) compared basking shark, Cetorhinus maximus, genetic diversity to other widespread pelagic elasmobranch species such as blacktip reef sharks and white sharks.…”

Comparative rates of growth of the Port Jackson shark throughout its southern Australian range

“…teleosts and elasmobranchs) is fundamental in fisheries science, providing the spatial framework for appropriate management and conservation strategies to maintain fish resources as well as preserving genetic diversity (Begg and Waldman 1999;Booke 1999;Abaunza 2008). Yet for elasmobranchs (sharks, rays and skates), few species have been examined for population structure via genetic analysis (Heist 2004a;Daly-Engel et al 2010), and limited focus has been given to utilising the elemental composition of the calcified tissues of elasmobranchs for testing patterns of structuring (Edmonds et al 1996;C. Izzo and B. M. Gillanders, unpubl.…”