爬行动物多父性生殖策略研究进展

动物生殖策略是多种多样的.对一个种群交配体系的调查有助于了解生殖模式的进化情况,并为一些濒危物种的保护计划提供理论依据,同时也为经济养殖动物的人工繁育提供理论支持.多父性( multiple paternity)现象是一种重要的生殖策略,在爬行类动物中普遍存在,并且在主要类群中多父性的水平也比较高,特别是多数有鳞类动物存在多父性现象的窝数可占到总检测窝数的50％以上,这种现象强烈地支持雌性存在混交的进化过程.本文对多父性产生的组织结构、可能机制和多父性的检测手段等进行综述,并对未来的研究方向提出了建议.     

Molecular determination of paternity in a natural population of the multiply mating polygynous lizard Eulamprus heatwolei

We studied the mating system of the southern water skink, Eulamprus heatwolei, during spring and summer (encompassing the breeding season) in a population in southeastern Australia. We examined potential attributes that might influence the mating system and male reproductive success including home range size, physical proximity of adults and body size, and then genotyped all mothers, offspring and potential sires. Home range overlap of both sexes was extensive, with adult females sharing the greatest amount of space with each other and adult males the least amount of space with each other. However, not all adults hold home ranges. We classified approximately one quarter of adult males as home range holders and the rest as 'floaters'. Adult females occupy home ranges more than males, with approximately three-quarters classified as home range holders. Home range ownership is not correlated with body size for either sex, however, male body size is positively correlated with the number of adult female home ranges that his home range overlaps and adult male home ranges are larger than those of females. We used microsatellite genotyping to assign paternities to 55 offspring from 17 litters and then compared this data with our home range and behavioural observations. This species displays extreme levels of multiple paternity given the small mean clutch size of three. Multiple paternity was confirmed in 11 (64.7%) of 17 clutches but three other clutches (for a total of 82.4%) also may display multiple paternity. A total of 30 offspring from 12 litters were assigned to 10 of the 32 genotyped adult males from our study site. Of these 10 adult males, half were home range holders. Five complete clutches and a total of 25 out of the 55 offspring could not be positively assigned to any male surveyed as part of the study and were attributed to floater males or resident males adjacent to our study site that had not been genotyped. While sample sizes are small, neither male home range ownership nor body size is significantly correlated with the number of paternities a male obtained. Our study suggests a polygynous mating system for this species.     

Discovery of four natural clones in a crayfish species Procambarus clarkii

Self-cloning is quite rare in shrimp, lobsters, crayfish and crabs. Here we report the discovery of four natural clones of red swamp crayfish (Procambarus clarkii), each containing 2-6 genetically identical individuals, during the genotyping of 120 individuals with five microsatellites. The four clones were heterozygote at most of the five microsatellite loci. Phylogenetic analysis using microsatellite genotypes suggests recent origin of the four clones. Sequencing a part of the mitochondrial gene Cox I confirmed that the four clones were from the species Procambarus clarkii.     

Multiple paternity in side-neck turtles Podocnemis expansa: evidence from microsatellite DNA data

Multiple paternity was found in two clutches of Podocnemis expansa using eight microsatellite loci. When loci were analysed separately a minimum of two males was estimated for nest N23, and three for nest C17. When all loci were combined, three patrilines were detected in N23, and six in C17. The distribution of full-sib cluster sizes indicated a disproportionate contribution of one male to clutch C17, consistent with possible sperm competition, or the mixing of leftover and newly acquired sperm. High mutation rates were detected at several loci. Multiple paternity has positive implications for this endangered species as it may slow the loss of genetic variability caused by drift. This is the first report of multiple paternity in the suborder Pleurodira.     

Geographic variation of multiple paternity in the American lobster, Homarus americanus

We studied the frequency of multiple paternity for American lobster (Homarus americanus) at three Canadian sites differing in exploitation rate and mean adult size. The probability of detecting multiple paternity using four microsatellite loci and 100 eggs per female was in excess of 99% under various scenarios of paternal contribution. Overall, 13% of the 108 examined females carried a clutch sired by two or three males. Multiple paternity was observed at the two most exploited sites (11% at Magdalen Islands and 28% at Grand Manan Island), whereas single paternity only was observed at the least exploited site (Anticosti Island). Within populations females with a clutch sired by more than one male tended to be smaller than females with a clutch sired by a single male. Based on these and other findings, we postulate a link between female promiscuity and sperm limitation in the American lobster.     

Historical,human, and environmental drivers of genetic diversity in the red swamp crayfish (Procambarus clarkii) invading the Iberian Peninsula

1. Patterns of genetic diversity in invasive populations can be modulated by a range of factors acting at different stages of the invasion process, including the genetic composition of the source population(s), the introduction history (e.g. propagule pressure), the environmental suitability of recipient areas, and the features of secondary introductions.
2. The North American red swamp crayfish, Procambarus clarkii, is one of the most widely introduced freshwater species worldwide. It was legally introduced into Spain twice, near the city of Badajoz in 1973 and in the Guadalquivir marshes in 1974. Thereafter the species rapidly colonised almost the entire Iberian Peninsula.
3. We used seven nuclear microsatellites to describe the genetic diversity and structure of 28 locations distributed across the Iberian Peninsula and to explain the expansion process of the red swamp crayfish. Additionally, we analysed the relationship between environmental suitability and genetic diversity of the studied locations.
4. The red swamp crayfish had a clear spatial genetic structure in the Iberian Peninsula, probably determined by the two independent introduction events in the 1970s, which produced two main clusters separated spatially, one of which was dominant in Portugal and the other in Spain.
5. The human-mediated dispersal process seemed to have involved invasion hubs, hosting highly genetically diverse areas and acting as sources for subsequent introductions. Genetic diversity also tended to be higher in more suitable environments across the Iberian Peninsula .
6. Our results showed that the complex and human-mediated expansion of the red swamp crayfish in the Iberian Peninsula has involved several long- and short-distance movements and that both ecological and anthropogenic factors have shaped the genetic diversity patterns resulting from this invasion process. Early detection of potential invasion hubs may help to halt multiple short-distance translocations and thus the rapid expansion of highly prolific invasive species over non-native areas.

     

The frequency of multiple paternity suggests that sperm competition is common in house mice (Mus domesticus)

Sexual selection is an important force driving the evolution of morphological and genetic traits. To determine the importance of male-male, postcopulatory sexual selection in natural populations of house mice, we estimated the frequency of multiple paternity, defined as the frequency with which a pregnant female carried a litter fertilized by more than one male. By genotyping eight microsatellite markers from 1095 mice, we found evidence of multiple paternity from 33 of 143. Evidence for multiple paternity was especially strong for 29 of these litters. Multiple paternity was significantly more common in higher-density vs. lower-density populations. Any estimate of multiple paternity will be an underestimate of the frequency of multiple mating, defined as the frequency with which a female mates with more than a single male during a single oestrus cycle. We used computer simulations to estimate the frequency of multiple mating, incorporating observed reductions in heterozygosity and levels of allele sharing among mother and father. These simulations indicated that multiple mating is common, occurring in at least 20% of all oestrus cycles. The exact estimate depends on the competitive skew among males, a parameter for which we currently have no data from natural populations. This study suggests that sperm competition is an important aspect of postcopulatory sexual selection in house mice.     

Multiyear multiple paternity and mate fidelity in the American alligator, Alligator mississippiensis

We examined multiple paternity during eight breeding events within a 10-year period (1995–2005) for a total of 114 wild American alligator nests in Rockefeller Wildlife Refuge in south-west Louisiana. Our goals included examining (i) within population variation in multiple paternity among years, (ii) variation in multiple paternity in individual females and (iii) the potential for mate fidelity. To accomplish this, in the current study, eggs were sampled from 92 nests over 6 years and analysed along with 22 nests from a previous 2-year study. Genotypes at five microsatellite loci were generated for 1802 alligator hatchlings. Multiple paternity was found in 51% of clutches and paternal contributions to these clutches were highly skewed. Rates of multiple paternity varied widely among years and were consistently higher in the current study than previously reported for the same population. Larger females have larger clutches, but are not more likely to have multiply sired nests. However, small females are unlikely to have clutches with more than two sires. For 10 females, nests from multiple years were examined. Seven (70%) of these females exhibited long-term mate fidelity, with one female mating with the same male in 1997, 2002 and 2005. Five females exhibiting partial mate fidelity (71%) had at least one multiple paternity nest and thus mated with the same male, but not exclusively. These patterns of mate fidelity suggest a potential role for mate choice in alligators.     

Genetic variation,multiple paternity,and measures of reproductive success in the critically endangered hawksbill turtle (Eretmochelys imbricata)

The Yucatán Peninsula in Mexico contains some of the largest breeding groups of the globally distributed and critically endangered hawksbill turtle (Eretmochelys imbricata). An improved understanding of the breeding system of this species and how its genetic variation is structured among nesting areas is required before the threats to its survival can be properly evaluated. Here, we genotype 1195 hatchlings and 41 nesting females at 12 microsatellite loci to assess levels of multiple paternity, genetic variation and whether individual levels of homozygosity are associated with reproductive success. Of the 50 clutches analyzed, only 6% have multiple paternity. The distribution of pairwise relatedness among nesting localities (rookeries) was not random with elevated within‐rookery relatedness, and declining relatedness with geographic distance indicating some natal philopatry. Although there was no strong evidence that particular rookeries had lost allelic variation via drift, younger turtles had significantly lower levels of genetic variation than older turtles, suggesting some loss of genetic variation. At present there is no indication that levels of genetic variation are associated with measures of reproductive success such as clutch size, hatching success, and frequency of infertile eggs.     

Detection of multiple paternity in the Kemp's ridley sea turtle with limited sampling

An important question in sea turtle biology is the number of males that contribute to the fertilization of a clutch of eggs. Previous studies on other sea turtle species have indicated little to no multiple paternity. We conclude here that female Kemp's ridleys, Lepidochelys kempi , are polyandrous. DNA from 26 mother and offspring groups was analysed at three microsatellite loci to identify paternal alleles. Three paternal alleles were observed among 14 of the clutches; four paternal alleles were observed among the offspring of an additional female. A maximum likelihood analysis not only rejects the model of single paternity, but also rejects the model of equal paternal contribution to the clutch. By explicitly addressing the high mutation rate of microsatellite markers, our analysis rejected mutation as the sole cause of multiple paternal alleles.     

Inter-population variation in multiple paternity and reproductive skew in the guppy

We use microsatellite loci to detail the multiple paternity patterns in broods from 10 wild populations of the guppy ( Poecilia reticulata ) found in Northern Trinidad. The populations span two major drainages comprising the Caroni and the Oropouche, and include sites that are characterized by either high or low predation. Across the populations the frequency of multiple paternity is high with 95% (range: 70%–100%) of broods having multiple sires. Broods have an average of 3.5 sires (range: 1–9) and a mixed-model analysis suggests that broods from high predation sites have marginally more sires than do those from low predation sites, but this is true only in the Oropouche drainage. There is no difference in sire number between predation sites in the Caroni drainage. Brood size, but not female body length, is correlated with the number of sires and the correlation cannot be attributed solely to the stochastic process associated with sperm competition and a 'fair raffle'. Within broods there is significant skew in reproductive success among males, which may reflect variation in sperm competitiveness or female choice. There is, however, no difference in the skew among populations from different predation regimes or drainages. Finally, high predation populations were characterized by increased genetic variability at the microsatellite loci, suggesting a larger effective population size. We discuss explanations for the high degree of multiple paternity but the general lack of any major differences among broods from ecologically different populations.     

Microsatellite markers and multiple paternity in the garter snake thamnophis sirtalis

Data from four microsatellite loci developed for the common garter snake, Thamnophis sirtalis, show that multiple paternity is common in a natural population on Beaver Island, Michigan. Six of eight litters tested, and all litters with five or more neonates, were multiply sired. At least triple paternity was documented in the largest litter examined (n = 13 neonates). Inheritance patterns and genotype frequencies in the wild population indicate the presence of null allele(s) at one of the microsatellite loci. Garter snakes are widely used in quantitative genetics research, and paternity testing is essential in studies that rely on sibling analysis.     

Eleven polymorphic microsatellites isolated from red swamp crayfish, Procambarus clarkii

Eleven microsatellites were isolated from a genomic DNA library enriched for CA- and GA-repeats, and were characterized in 48 individuals of red swamp crayfish Procambarus clarkii. All 11 microsatellites were polymorphic with an average of allele number of 6.6 per locus. Genotypic distributions of these 11 markers were found to be in conformance with the expectations of Hardy-Weinberg equilibrium. All 11 markers were unlinked. These markers are being used to study the invasion routine, genetic diversity and population structure of the species P. clarkii.     

Evidence of multiple paternity in spiny dogfish (Squalus acanthias) broods based on microsatellite analysis

An understanding of alternative mating systems is a fundamental requirement for the effective management of vulnerable species. Microsatellite analysis of spiny dogfish Squalus acanthias broods from the north‐west Atlantic provides novel evidence of polyandry in this species.     

Multiple paternity and population genetic structure in natural populations of the poeciliid fish, Heterandria formosa

Heterandria formosa Agassiz, exhibits internal fertilization, internal brooding of embryos, sperm storage and an extreme level of superfetation. In this study we used microsatellite markers to examine variation among seven populations that exhibited significant variance in their histories of population density. We found that the populations were genetically distinct and that the heterozygosity increased as population density increased. We also examined paternity in three of those populations and found that the number of sires per female and the number of sires per brood increased with population density. Overall, the rates of multiple paternity are quite low relative to other species. The correlations with population density suggest that contact rates play a critical role in the breeding system in this species but the low rates of multiple paternity suggest that females may exert control over fertilization of their ova.     

Multiple paternity in clutches of common lizard Lacerta vivipara: data from microsatellite markers

The common lizard (Lacerta vivipara) is a small live-bearing lacertid that reproduces once a year. In order to document the poorly known mating system of this species, we present here an assessment of multiple paternity using microsatellite markers. Paternities were established within 122 clutches belonging to two wild populations from contrasted areas and to four seminatural enclosed populations. The proportion of multiply sired clutches was found to be very high (between 50.0% and 68.2%) and similar among populations, which suggests that the mating system of this species may be insensitive to environmental and population conditions.     

Multiple paternity in an aggregate breeding amphibian: the effect of reproductive skew on estimates of male reproductive success

Aggregate, or explosive, breeding is widespread among vertebrates and likely increases the probability of multiple paternity. We assessed paternity in seven field-collected clutches of the explosively breeding spotted salamander (Ambystoma maculatum) using 10 microsatellite loci to determine the frequency of multiple paternity and the number of males contributing to a female's clutch. Using the Minimum Method of allele counts, multiple paternity was evident in 70% of these egg masses. Simple allele counts underestimate the number of contributing males because this method cannot distinguish multiple fathers with common or similar alleles. Therefore, we used computer simulations to estimate from the offspring genotypes the most likely number of contributing fathers given the distributions of allele frequencies in this population. We determined that two to eight males may contribute to A. maculatum clutches; therefore, multiple paternity is a common strategy in this aggregate breeding species. In aggregate mating systems competition for mates can be intense, thus differential reproductive success (reproductive skew) among males contributing to a female's clutch could be a probable outcome. We use our data to evaluate the potential effect of reproductive skew on estimates of the number of contributing males. We simulated varying scenarios of differential male reproductive success, ranging from equal contribution to high reproductive skew among contributing sires in multiply sired clutches. Our data suggest that even intermediate levels of reproductive skew decrease confidence substantially in estimates of the number of contributing sires when parental genotypes are unknown.     

Multiple paternity in the European hedgehog

Previous observations have suggested that European hedgehogs Erinaceus europaeus are promiscuous, although there have been no direct studies of the mating system to confirm this. In this study, the genetic mating system of the European hedgehog was assessed by analysing mother–offspring groups using six polymorphic microsatellite loci. Evidence of multiple paternity was found in two of five litters analysed and therefore demonstrates the occurrence of polyandry in wild populations of hedgehogs.     

Niche conservatism and the potential for the crayfish Procambarus clarkii to invade South America

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