What Is Intrauterine Cannibalism (as Applied to Sand Tiger Sharks)?
Biol Lett. 2013 Jun 23; ix(three): 20130003.
The behavioural and genetic mating organization of the sand tiger shark, Carcharias taurus, an intrauterine cannibal
Demian D. Chapman
1School of Marine and Atmospheric Science, Institute for Ocean Conservation Science, Stony Brook University, Stony Brook, NY 11794, USA
Sabine P. Wintner
2Kwa-Zulu Natal Sharks Board and Biomedical Resource Unit, University of KwaZulu-Natal, Durban 4056, Southward Africa
Debra L. Abercrombie
oneSchoolhouse of Marine and Atmospheric Science, Plant for Ocean Conservation Science, Stony Brook University, Stony Brook, NY 11794, U.s.a.
Jimiane Ashe
1Schoolhouse of Marine and Atmospheric Science, Institute for Ocean Conservation Science, Stony Brook University, Stony Brook, NY 11794, USA
Andrea M. Bernard
3Guy Harvey Research Plant, Oceanographic Middle, Nova Southeastern Academy, Dania Embankment, FL 33004, USA
Mahmood S. Shivji
3Guy Harvey Inquiry Institute, Oceanographic Centre, Nova Southeastern University, Dania Embankment, FL 33004, USA
Kevin A. Feldheim
4Pritzker Laboratory for Molecular Systematics and Evolution, Field Museum of Natural History, 1400 South Lake Shore Drive, Chicago, IL 60605, USA
Received 2013 Jan 2; Accepted 2013 Apr 11.
Abstruse
Sand tiger sharks (Carcharias taurus) have an unusual mode of reproduction, whereby the start embryos in each of the paired uteri to achieve a certain size ('hatchlings') swallow all of their smaller siblings during gestation ('embryonic cannibalism' or EC). If females commonly mate with multiple males ('behavioural polyandry') then litters could initially have multiple sires. It is possible, however, that EC could exclude of all but i of these sires from producing offspring thus influencing the species genetic mating organization ('genetic monogamy'). Hither, we use microsatellite DNA profiling of mothers and their litters (n = 15, from two to nine embryos per litter) to quantify the frequency of behavioural and genetic polyandry in this system. We conservatively gauge that ix of the females we examined (sixty%) were behaviourally polyandrous. The genetic mating system was characterized by assessing sibling relationships between hatchlings and revealed only twoscore per cent genetic polyandry (i.eastward. hatchlings were total siblings in threescore% of litters). The discrepancy stemmed from three females that were initially fertilized by multiple males but only produced hatchlings with 1 of them. This reveals that males can exist excluded even later fertilizing ova and that some instances of genetic monogamy in this population arise from the reduction in litter size by EC. More research is needed on how ambiguous post-copulatory and postal service-zygotic processes contribute to determining paternity and bridging the behavioural and genetic mating systems of viviparous species.
Keywords: polyandry, monogamy, adelphophagy
1. Introduction
Animal mating systems can be parsed into the behavioural component, describing copulation patterns, and the genetic component that describes the realized distribution of parentage [1]. Almost broods of internally fertilizing animals showroom multiple paternity, indicating a genetic mating system that includes behavioural polyandry (i.east. females mating with multiple males; [1]). In a few species or populations, yet, single paternity of broods is more common ('genetic monogamy' [ii–four]). Although multiple paternity provides definitive proof of behavioural polyandry and demonstrates some level of concordance between the behavioural and genetic mating systems, genetic monogamy is ambiguous with regard to the underlying mating behaviour. Genetic monogamy can effect from a female only mating with ane male person, simply it can also ascend after post-copulatory competitive or selective processes let i of several mating partners to monopolize paternity [1,v].
The sand tiger shark, Carcharias taurus, has a remarkable reproductive style in which the behavioural and genetic mating organisation are decoupled by embryonic cannibalism ('EC'), potentially enabling post-zygotic processes to ultimately make up one's mind paternity of the litter. Female person sand tigers ovulate for several months, with ova entering the upper oviduct where fertilization occurs [6]. Single or a few fertilized ova are then encapsulated so settle in either the right or left of the paired uteri. The first embryo in each uterus to 'hatch' from its egg capsule, occurring when it reaches a length of approximately 55–lx mm, is called the 'hatchling' [6]. Soon after, the approximately 100 mm hatchling gain to attack, kill and eventually consume all of its younger siblings, achieving exponential growth over this menstruation [vi]. The hatchling then has sole access to unfertilized ova accumulated in the uterus, which are consumed for much of the rest of gestation ('oophagy'). Term litters consist of a pair of hatchlings, 1 from each uterus, that are built-in at such large sizes (approx. 950–1250 mm) that they have few predators [vi].
The unusual developmental mode of sand tigers raises interesting questions near how EC influences the species genetic mating system (i.e. distribution of parentage). The behavioural mating system of female sand tigers is not known, simply if behavioural polyandry is common then it is possible that they initially gestate litters sired past multiple males similar to many other animals [1,2,five]. Dissimilar most other animals, however, the majority of embryonic sand tiger sharks are not carried to term because of EC [six]. This raises the possibility that some sires that initially fertilize ova are excluded because all of their progeny are consumed by the hatchlings. From a mating arrangement perspective, this could oftentimes consequence in genetic monogamy despite behavioural polyandry by females. We therefore used microsatellite Dna profiling to deport the offset parentage report of a species with EC, which may be an important determinant of the genetic mating organisation.
2. Cloth and methods
Gravid sand tigers were obtained from mortality events associated with protective embankment meshing operations in Richards Bay, South Africa (28°48′0″ S, 32°vi′0″ E) from 2008 to 2012. Tissue samples from mothers and their embryos were stored at room temperature in 95 per cent ethanol, as were samples from developed males and females collected in the aforementioned area. Microsatellite genotyping of each private at 10 polymorphic loci (9–32 alleles per locus) is described in the electronic supplementary material. The parental exclusion probability of this panel of markers was over 99.ix per cent if one parent is known as calculated in Gerud 5. ii.0 [7] using allele frequencies observed in sampled adults. Genotypes of individuals used in this study can be found in the electronic supplementary material.
We showtime aimed to characterize the behavioural mating system of this population by estimating the frequency of behavioural polyandry. Like nearly all sharks at that place are no observations of free-living sand tigers mating. We can therefore merely guess the frequency of behavioural polyandry using genetic parentage analysis. This is necessarily conservative considering it just detects polyandry that results in multiple paternity. Since diploid males tin can laissez passer a maximum of two alleles to their offspring at each locus, more than ii paternal alleles in a litter reveals the presence of multiple sires (i.east. the paternal allele count method). This can only exist tested in litters composed of three or more embryos (i.e. litters sampled prior to the end of the EC phase of evolution). For litters composed only of a pair of hatchlings (i.due east. litters sampled after EC is completed), we calculated the probabilities that the pair were either full siblings (same father and therefore genetic monogamy) or maternal one-half siblings (different fathers, proving both behavioural and genetic polyandry) in the plan ML-Relate [8]. ML-Relate'south hypothesis testing selection was used to assess the probability of each sibling relationship. These probabilities were generated from 10 000 simulated genotypes using population allele frequencies estimated using adults sampled in the study area. We study which human relationship had the highest probability, since these are the only two possibilities. In summary, we considered a female person to exist behaviourally polyandrous when its litter had more than ii paternal alleles or, when there were simply 2 embryos bachelor, if they were maternal half siblings.
The genetic mating system of sand tigers is determined by the paternity of hatchlings, as they are the but embryos that survive to term and contribute to the next generation. Equally there are but two hatchlings per litter, we used ML-Relate to decide whether they were full or maternal half siblings as described above. The identity of hatchlings in litters composed of more than two embryos was obvious in the litters nosotros examined considering of their larger sizes relative to their siblings, most of which were also still encapsulated (figure 1). In summary, we report ii carve up mating system parameters. The frequency of behavioural polyandry was conservatively estimated by examining all embryos available in each litter (the behavioural mating organisation). The frequency of genetic polyandry was estimated based on the relationship of each pair of hatchlings (the genetic mating organisation).
Size differential betwixt the hatchling (H) and an embryo (E) from the same uterus in ane of the litters we sampled. In all five litters sampled prior to EC, we observed a similar size differential.
3. Results and give-and-take
Gravid females are rarely captured in the beach meshing programme, but nosotros were able to collect xv litters (mothers and embryos) from 2007 to 2012. 20-3 additional adult males and females also captured in Richard's Bay were used to gauge population allele frequencies. Five of the 15 litters were collected prior to the completion of EC and were composed of six to 9 embryos each (table 1). These were amenable to using the paternal allele count method. All of them exhibited three or four paternal alleles at four to eight of the 10 profiled loci, conclusive evidence that these females had mated with at least two males each (table 1). The remaining litters (northward = ten) were sampled after EC was finished and the hatchlings were all that remained of the litter. Four hatchling pairs shared no paternal alleles, which is highly unlikely if they were full siblings (tabular array i). We conclude that they were maternal half siblings (i.e. had unlike fathers). We therefore found evidence of behavioural polyandry in nine out of the fifteen litters we examined and conservatively estimate that 60 per cent of the females we sampled, including all 5 of those sampled prior to the completion of EC, were behaviourally polyandrous.
Table 1.
Results of genetic analyses of sand tiger litters (Ct001–Ct015). N embryos is the litter size. PAC, paternal allele counts. The relationship between the hatchlings as assessed in ML-Relate is provided under the following headings: Put FS, the simulation-based probability that the alternative human relationship (half-siblings) meliorate fits the hatchling genotypes than the putative relationship of full-siblings. If this value is depression then the putative relationship is virtually likely to be true; Put HS, the simulation-based probability that the alternative relationship (full-siblings) better fits the hatching genotypes than the putative relationship of half-siblings. northward.a., exam non applicative; ?, mating behaviour uncertain. 'Behavioural polyandry' was established past either PAC and/or when hatchlings were most likely to be half-siblings. 'Genetic polyandry' is established when hatchling were well-nigh likely to exist one-half-siblings.
| litter | hatchlings | |||||
|---|---|---|---|---|---|---|
| female | n embryos | PAC | Put FS | Put HS | behavioural polyandry | genetic polyandry |
| Ct001 | 2 | n.a. | 0.84 | 0.02 | yep | aye |
| Ct002 | 2 | due north.a. | 0.002 | 0.65 | ? | no |
| Ct003 | 2 | n.a. | 0.45 | 0.034 | aye | yep |
| Ct004 | 2 | n.a. | 0.01 | 0.45 | ? | no |
| Ct005 | 2 | n.a. | 0.01 | 0.45 | ? | no |
| Ct006 | 2 | n.a. | 0.132 | 0.999 | ? | no |
| Ct007 | 2 | north.a. | 0.685 | 0.009 | yes | yes |
| Ct008 | 2 | n.a. | 0.79 | 0.005 | yes | yes |
| Ct009 | 2 | northward.a. | 0.032 | 0.34 | ? | no |
| Ct010 | 2 | n.a. | 0.003 | 0.85 | ? | no |
| Ct011 | 7 | 2–iv/locus | 0.32 | 0.06 | yes | yes |
| Ct012 | 8 | 2–4/locus | 0.34 | 0.05 | yeah | aye |
| Ct013 | six | ii–4/locus | 0.007 | 0.52 | yes | no |
| Ct014 | 9 | two–4/locus | 0.005 | 0.56 | yes | no |
| Ct015 | vii | 2–4/locus | 0.001 | 0.59 | yes | no |
To assess the genetic mating system of sand tigers, we calculated the probabilities that hatchling pairs sampled were full or half siblings for all 15 litters. We establish that the hatchling in 6 of the 15 were maternal one-half siblings (40% genetic polyandry; table 1). The remaining nine females (60%) were genetically monogamous (tabular array 1). In half dozen of these, we sampled only hatchlings and therefore cannot resolve whether or not the female was behaviourally polyandrous. Yet, in the iii cases where we sampled both hatchlings and smaller embryos paternal allele counts proved that the female was behaviourally polyandrous. These 3 cases demonstrate that some sires are excluded by EC, and private cases of genetic monogamy sometimes occur despite behavioural polyandry.
It is widely known that behavioural polyandry can initiate post-copulatory competition between males in internally fertilizing species [i]. The existence of behavioural polyandry suggests there is sperm contest in sand tigers, which corresponds with the observation that males of this species store larger volumes of sperm than other sharks [9]. EC broadens sexual selection beyond mail-copulatory competition to simply fertilize ova considering information technology generates contest to fertilize specific ova: those that are almost likely to go hatchlings. Fertilizing the earliest ova is likely to be important considering the earliest embryos to settle in each uterus have a head kickoff when it comes to reaching hatchling size [6]. Male sand tigers are reported to engage in mate guarding behaviour in captivity, with a dominant male physically excluding rivals from females until after it had copulated [ten]. If this is representative of natural behaviour, then mate guarding could have evolved to maximize the probability of fertilizing the earliest ova and/or to filibuster subsequent fertilizations by other males. Sexual pick is broadened still further in cases where there are a few similar-sized embryos in each uterus as they arroyo hatching [vi]. In this situation, any trait that enhances the competitive ability of the embryo itself would exist bailiwick to positive selection. For example, individual growth rate could determine which of several similar-sized embryos would hatch first and swallow its younger siblings, presumably selecting for males to comport genes that promote rapid embryonic growth. It is also possible to envision how this type of selection may have influenced the precocious development of eyes and teeth that occurs in embryonic sand tigers, which enhances their power to locate and consume their siblings [half dozen].
Female person sand tigers make an extremely big energetic investment in two offspring per gestation [6]. Although female sharks, including sand tigers, can either cooperate or engage in avoidance behaviours during copulation attempts information technology is thought that they practise non have absolute control over mate choice or mating frequency [xi]. EC may increment the probability that uniform and/or competitively superior males (in terms of behavioural dominance, sperm competition or producing competitive embryos) sire the hatchlings, even if females are unable to control mating frequency or outwardly appraise mate quality. The 'convenience polyandry hypothesis' postulates that females may accept multiple mating partners simply because the costs of resistance exceed the costs of accepting superfluous copulation [12]. EC may allow female sand tigers to appoint in convenience polyandry later on mating with preferred males without really investing in embryos from these superfluous copulations.
The original envisioning of sexual choice was based on the competition that occurred betwixt males for mates [13]. A century later, information technology was recognized that sexual selection continues later copulation when sperm from different males compete to fertilize ova [5]. While multiple male sand tigers commonly fertilize a unmarried female, EC sometimes excludes all simply one of them from gaining offspring. This system highlights that competition and sexual selection can nevertheless occur afterward fertilization. Although EC is rare in nature [half dozen], competition betwixt embryos is mutual in viviparous species and may lead to bloodshed during or immediately following gestation [one]. This competition can play an important and probably underappreciated role in determining male fitness.
Acknowledgements
This research was supported past operational funds to the Plant for Body of water Conservation Science from The Pew Charitable Trusts, private donors to the Institute for Ocean Conservation Science and the Guy Harvey Inquiry Found. Genetic information were collected in the Field Museum'due south Pritzker Laboratory for Molecular Systematics and Evolution operated with support from the Pritzker Foundation.
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