Polyandry in dragon lizards: inbred paternal genotypes sire fewer offspring

Multiple mating in female animals is something of a paradox because it can either be risky (e.g., higher probability of disease transmission, social costs) or provide substantial fitness benefits (e.g., genetic bet hedging whereby the likelihood of reproductive failure is lowered). The genetic relatedness of parental units, particularly in lizards, has rarely been studied in the wild. Here, we examined levels of multiple paternity in Australia's largest agamid lizard, the eastern water dragon (Intellagama lesueurii), and determined whether male reproductive success is best explained by its heterozygosity coefficient or the extent to which it is related to the mother. Female polyandry was the norm: 2/22 clutches (9.2%) were sired by three or more fathers, 17/22 (77.2%) were sired by two fathers, and only 3/22 (13.6%) clutches were sired by one father. Moreover, we reconstructed the paternal genotypes for 18 known mother–offspring clutches and found no evidence that females were favoring less related males or that less related males had higher fitness. However, males with greater heterozygosity sired more offspring. While the postcopulatory mechanisms underlying this pattern are not understood, female water dragons likely represent another example of reproduction through cryptic means (sperm selection/sperm competition) in a lizard, and through which they may ameliorate the effects of male‐driven precopulatory sexual selection.     

No evidence of sperm selection by female common shrews.

There is currently much interest in the suggestion that females are capable of post-copulatory (or cryptic) choice for male genetic compatibility. Here, I investigate this idea using data from mixed-paternity litters of the common shrew (Sorex araneus). Females of this species are highly promiscuous and, in natural populations, regularly incur costs of inbreeding by mating with close relatives. Selection should therefore favour female ability for sperm selection on the basis of male relatedness. No evidence was found in support of this idea. Relative number of offspring sired within mixed paternity litters was not significantly correlated with genetic similarity of males to the female mated. Relative fertilization success was, however, significantly related to male epididymal sperm counts. I conclude that most variation in relative fertilization success of male common shrews can be explained in terms of sperm competition, and that females of this species may not be capable of sperm selection.     

圈养猞猁多雄交配雄性的成功繁殖

研究了笼养猞猁多雄交配的结果以及雄性的成功繁殖。雄兽与发情雌兽随机配对,其繁殖成功(所产生的后代数量)不取决于与雌兽的交配顺序、交配次数与持续时间、遗传关系或雄兽的行为特征,但似乎取决于精子质量,特别是取决于形态正常精子的百分率。繁殖成功的雄兽比其竞争对手具有更多的形态正常的精子,似乎更能成功地诱发交配雌兽的排卵。证实了4窝(占总窝数的20%)幼兽的双重父亲身份。在所有情形下, 2雄1雌的交配间隔为24h 。     

Parentage, reproductive success and breeding behaviour in the greater horseshoe bat (Rhinolophus ferrumequinum)

Female greater horseshoe bats form maternity colonies each summer in order to give birth and raise young. During the mating period, females visit males occupying territorial sites, copulation takes place and sperm are stored until ovulation occurs, normally in April. Using microsatellite markers and a likelihood method of parentage analysis, we studied breeding behaviour and male reproductive success over a five-year period in a population of bats in south-west Britain. Paternity was assigned with 80% confidence to 44% of young born in five successive cohorts. While a small annual skew in male reproductive success was detected, the variance increased over five years due to the repeated success of a few individuals. Mating was polygynous, although some females gave birth to offspring sired by the same male in separate years. Such repeated partnerships probably result from fidelity for either mating sites or individuals or from sperm competition. Females mated with males born both within and outside their own natal colony; however, relatedness between parents was no less than the average recorded for male female pairs. Gene flow between colonies is likely to be primarily mediated by both female and male dispersal during the mating period rather than more permanent movements.     

Longevity of the freshwater anostracan Streptocephalus mackini (Crustacean: Anostraca) in relation to food (Chlorella vulgaris) concentration

SUMMARY 1. Temporary ponds are inhabited by a variety of invertebrates, of which anostracans are an important group. We studied the lifetables of male and female anostracan Streptocephalus mackini at 3 algal concentrations (0.5 × 10⁶, 1.0 × 10⁶ and 1.5 × 10⁶ cells mL⁻¹).
2. Regardless of sex, S. mackini showed better survivorship at lower food levels. The longest average lifespan observed was 85 ± 2 days for males fed Chlorella at 0.5 × 10⁶ cells mL⁻¹.
3. Both net reproductive rate and generation time decreased with increasing food level. The highest net reproductive rate was about 120 cysts per female. The longest generation time of about 40 days, observed at 0.5 × 10⁶ cells mL⁻¹, was more than three times that at 1.5 × 10⁶ cells mL⁻¹.
4. The rate of population increase ( r ) was nearly the same (0.31 ± 0.06) at high (1.5 × 10⁶ cells mL⁻¹) and intermediate (1.0 × 10⁶ cells mL⁻¹) food levels. The r -value at low food level (0.5 × 10⁶ cells mL⁻¹ of Chlorella ) was 0.20 ± 0.01 per day.     

Reproductive characteristics of the male herring in the northern Baltic Sea

The gonad weight and gonadosomatic index of the male Baltic herring Clupea harengus membras L., were highest at the beginning of the reproductive season (April/May), the values decreasing towards the end of it (July/August) during 1988–1991. The decline could not be explained by fish size but may have been due to fish condition. A high individual variation was typical for both gonad weights and gonadosomatic indices in fish of the same size and maturity stage. The mean density of sperm cells was significantly higher in June (34·9 × 10⁹ ml⁻¹) than in July (19·2 × 10⁹ ml⁻¹, Mann-Whitney U= 17; P<0·05), the variation among the males being high in both groups. Electron microscope analysis showed a severe disruption of the mitochondrial elements in males spawning at 22°C.     

Are non-reproductive male highveld mole-rats, Cryptomys hottentotus pretoriae physiologically suppressed while in the confines of the natal colony?

The highveld mole-rat, Cryptomys hottentous pretoriae is a social, subterranean, co-operative breeder with a high reproductive skew. The relationship between reproductive status and reproductive physiology in male highveld mole-rats was investigated. Testicular morphometrics, histological parameters, plasma testosterone concentrations and sperm motility parameters were studied in 31 males (14 reproductive and 17 non-reproductive males). Reproductive males were significantly larger than non-reproductive males, with testicular mass and volume corrected for body mass considerably larger for the reproductive males. Circulating plasma testosterone concentrations of reproductive males were not significantly higher than non-reproductive males (reproductive males 10.3±1.8 nmol l⁻¹ vs non-reproductive males 7.3±1.74 nmol l⁻¹). Sperm motility parameters were measured, but no significant differences were found between reproductive and non-reproductive males. All 14 reproductive males had motile sperm, whereas 13 of the 17 (76%) of non-reproductive males possessed motile sperm. A typical ejaculate of a reproductive male contains 48.3% motile sperm characterized by a high percentage of flagellar defects, whereas the non-reproductive male has an ejaculate containing 45.6% motile sperm with a high percentage of head defects. It is apparent that non-reproductive males are not physiologically suppressed from reproducing. Moreover, the non-reproductive males are excluded from incestuous matings as a result of being the offspring of the reproductive female.     

Sperm production, storage, and the synchronization of male and female reproductive cycles in the iteroparous, stripe-faced dunnart (Sminthopsis macroura; Marsupialia): relationship to reproductive strategies within the Dasyuridae

Seasonal changes in the number and distribution of spermatozoa in males, and annual changes in the distribution of litters and embryos in females were examined in the iteroparous dasyurid marsupial, Sminthopsis macroura , in captivity. Total number of sperm in the testis (0.53 × 10⁶ sperm/testis) and epididymidis (0.54 × 10⁶ sperm/epididymidis) were extremely low when compared with those in other marsupials and eutherian mammals. Testicular sperm production and epididymal sperm reserves were high between May and October and declined to a minimum in March. These changes reflected monthly changes in testicular and epididymal weight and testis morphology. Data on changing epididymal sperm distribution suggest that sperm storage in the cauda epididymidis is limited and that few sperm are required for successful insemination. Litters were born between June and January, with most litters occurring between July and October. Second pregnancies occurred between October and January, with a peak in December. The data indicate that the timing of mating activity and litter production by S. macroura correspond very closely with the period of maximum sperm production by males. The synchrony of these events contrasts dramatically with that of similar-sized semelparous dasyurid species. It is hypothesized that testicular failure prior to the mating season, copulatory behaviour, and possibly male die-off in dasyurid marsupials are related to the degree of competition between males for mates and, hence, population density and environmental predictability. These data suggest that intermale sperm competition is affected by the periods of female receptivity and the length of sperm storage in the female reproductive tract. Fundamental differences in the reproductive strategies of iteroparous and semelparous dasyurid marsupials are discussed.     

The more the better – polyandry and genetic similarity are positively linked to reproductive success in a natural population of terrestrial salamanders (Salamandra salamandra)

Although classically thought to be rare, female polyandry is widespread and may entail significant fitness benefits. If females store sperm over extended periods of time, the consequences of polyandry will depend on the pattern of sperm storage, and some of the potential benefits of polyandry can only be realized if sperm from different males is mixed. Our study aimed to determine patterns and consequences of polyandry in an amphibian species, the fire salamander, under fully natural conditions. Fire salamanders are ideal study objects, because mating, fertilization and larval deposition are temporally decoupled, females store sperm for several months, and larvae are deposited in the order of fertilization. Based on 18 microsatellite loci, we conducted paternity analysis of 24 female‐offspring arrays with, in total, over 600 larvae fertilized under complete natural conditions. More than one‐third of females were polyandrous and up to four males were found as sires. Our data clearly show that sperm from multiple males is mixed in the female's spermatheca. Nevertheless, paternity is biased, and the most successful male sires on average 70% of the larvae, suggesting a ‘topping off’ mechanism with first‐male precedence. Female reproductive success increased with the number of sires, most probably because multiple mating ensured high fertilization success. In contrast, offspring number was unaffected by female condition and genetic characteristics, but surprisingly, it increased with the degree of genetic relatedness between females and their sires. Sires of polyandrous females tended to be genetically similar to each other, indicating a role for active female choice.     

Early male reproductive advantage,multiple paternity and sperm storage in an amphibian aggregate breeder

We tested whether the order in which males encounter females affects reproductive fitness in spotted salamanders (Ambystoma maculatum). Using mating chambers in the field, we allowed one male access to a female before a second male. We then used four microsatellite markers in paternity analyses of the resulting larvae. First males sired a significantly larger number of offspring than second males, suggesting that male reproductive success is greatly enhanced by early arrival at breeding ponds. Multiple paternity was common among clutches, and frequently larvae were assigned to unidentified males that had not been in the chambers. Sperm from these males had either been stored by females for a year or obtained more recently at other breeding sites.     

Sperm allocation in the three-spined stickleback

Male three-spined stickleback Gasterosteus aculeatus have a fixed amount of sperm during the breeding season because spermatogenesis is inhibited at this time. A method was developed to estimate ejaculate size in situ by removing the sperm from the male's nest. The reliability of the method was tested using known numbers of sperm. In their first mating, males ejaculated 11·64 × 10⁶ sperm (median), representing c. 5% of the male's sperm store (median 27·88 × 10⁷ sperm). The amount of sperm in the testes was significantly reduced in males that had mated several times (median 8·09 × 10⁷). Additionally, ejaculate size was smaller in these experienced males (median 8·79 × 10⁵). Heavier and larger fish invested absolutely and relatively more sperm in a mating than did lighter and smaller fish. Ejaculate size did not correlate with the mass of the egg clutch.     

Insights into the mating habits of the tiger salamander (Ambystoma tigrinum tigrinum) as revealed by genetic parentage analyses

Among urodeles, ambystomatid salamanders are particularly amenable to genetic parentage analyses because they are explosive aggregate breeders that typically have large progeny arrays. Such analyses can lead to direct inferences about otherwise cryptic aspects of salamander natural history, including the rate of multiple mating, individual reproductive success, and the spatial distribution of clutches. In 2002, we collected eastern tiger salamander (Ambystoma tigrinum tigrinum) egg masses (> 1000 embryos) from a approximately 80 m linear transect in Indiana, USA. Embryos were genotyped at four variable microsatellite loci and the resulting progeny array data were used to reconstruct multilocus genotypes of the parental dams and sires for each egg mass. UPGMA analysis of genetic distances among embryos resolved four instances of egg mass admixture, where two or more females had oviposited at exactly the same site resulting in the mixing of independent cohorts. In total, 41 discrete egg masses were available for parentage analyses. Twenty-three egg masses (56%) consisted exclusively of full-siblings (i.e. were singly sired) and 18 (44%) were multiply sired (mean 2.6 males/clutch). Parentage could be genetically assigned to one of 17 distinct parent pairs involving at least 15 females and 14 different males. Reproductive skew was evident among males who sired multiply sired clutches. Additional evidence of the effects of sexual selection on male reproductive success was apparent via significant positive correlations between male mating and reproductive success. Females frequently partitioned their clutches into multiple discrete egg masses that were separated from one another by as many as 43 m. Collectively, these data provide the first direct evidence for polygynandry in a wild population of tiger salamanders.     

Sexual selection,multiple mating and paternity in grey mouse lemurs,Microcebus murinus

Sexual selection theory predicts that the relative importance of dominance between males for access to females depends on the potential to monopolize oestrous females. We examined the relationship between male dominance, mating behaviour and reproductive success in a promiscuous, nocturnal primate species, the grey mouse lemur, in captivity, to test the predictions derived for different competitive regimes between males. We also investigated the relationship between male age, relatedness between mates and reproductive success. Dominance could be established in the majority of the study groups and dominant males mated more frequently than subdominant males. Dominant males, however, fathered only half of the infants born in the study groups, although in principle the captive conditions allowed males to monopolize mates. Multiple mating was observed or deduced from the paternity data in the majority of groups. For the first time in primates we detected one definite case of multiple paternity. Younger males sired more than half of the offspring. We conclude that contest competition between males is unlikely to be the primary factor predicting the reproductive outcome whereas female choice and sperm competition are likely to be effective in this seasonal breeder.     

Experimental Infection of Nosema sp. Ghose in an Unnatural Host Lesioderma sericorne

ABSTRACT. Various doses of a microsporan parasite, Nosema sp., were fed to third and fourth instar larvae of Lesioderma sericorne that infested different types of stored grains. A spore dose of 3 × 10³ spores/individual resulted in a 39% infection rate, reduction in larval and adult weights, and mean spore concentrations of 1.28 ± 0.2 × 10⁸ spores/larva and 1.1 ± 0.2 × 10⁸ spores/adult. At the above dose, mortality was not well marked (about 35% in larvae and 25% in adults). At 3 × 10⁴ spores/individual, the rate of mortality increases to 80% in larvae and 60% in adults. However, more of the pest population (88% of larvae and 73% of adults) died at a dose of 3 × 10⁵ spores/individual. This dose produced mean spore concentrations of 3.91 ± 0.2 × 10⁸ spores/larva and 2.89 ± 0.2 × 10⁸ spores/adult. Insect death was caused by heavy damage to gut epithelia and fat bodies.     

Induction of maturation and spermiation in the male European eel: assessment of sperm quality throughout treatment

Weekly injections of human chorionic gonadotropin (hCG; 1·5 IU g⁻¹ W ) induced spermiation in 87–100% farmed male European eels Anguilla anguilla over a 10-week period, producing 3 ml (100 g)⁻¹ milt volume, at 1˙4×10⁹ spermatozoa ml⁻¹ sperm mobility peaked in ninth week of treatment with 97% of males with motile sperm. Gonadotropin-treated males showed earlier but similar morphological changes to control males. Whereas higher sperm density was obtained 6 h after hCG administration, higher percentage of motile cells and longer sperm mobility were observed 24 h after the treatment indicating that this is the optimum time to obtain good sperm after the hormonal induction. Several monounsaturated fatty acids in sperm increased significantly from week 5 to 9 of treatment (when highest volume, density and mobility of milt were recorded), whereas eicosapentaenoic acid (EPA), docosahexaenoic acid (DHA) and total n-3 polyunsaturated fatty acids (PUFAs) were significantly reduced. Fatty acid levels returned to initial values after 13 weeks of treatment. These results are in agreement with the reduction of n-3 PUFAs recently observed in the ovary of female Japanese eel during artificial maturation, and an attempt is made to suggest a physiological explanation of its possible relation with sperm quality.     

Factors influencing paternity success in Antechinus agilis: last‐male sperm precedence,timing of mating and genetic compatibility

We describe the patterns of paternity success from laboratory mating experiments conducted in Antechinus agilis, a small size dimorphic carnivorous marsupial (males are larger than females). A previous study found last‐male sperm precedence in this species, but they were unable to sample complete litters, and did not take male size and relatedness into account. We tested whether last‐male sperm precedence regardless of male size still holds for complete litters. We explored the relationship between male mating order, male size, timing of mating and relatedness on paternity success. Females were mated with two males of different size with either the large or the small male first, with 1 day rest between the matings. Matings continued for 6 h. In these controlled conditions male size did not have a strong effect on paternity success, but mating order did. Males mating second sired 69.5% of the offspring. Within first mated males, males that mated closer to ovulation sired more offspring. To a lesser degree, variation appeared also to be caused by differences in genetic compatibility of the female and the male, where high levels of allele‐sharing resulted in lower paternity success.     

Effects of ovarian fluid and genetic differences on sperm performance and fertilization success of alternative reproductive tactics in Chinook salmon

In many species, sperm velocity affects variation in the outcome of male competitive fertilization success. In fishes, ovarian fluid (OF) released with the eggs can increase male sperm velocity and potentially facilitate cryptic female choice for males of specific phenotypes and/or genotypes. Therefore, to investigate the effect of OF on fertilization success, we measured sperm velocity and conducted in vitro competitive fertilizations with paired Chinook salmon (Oncorhynchus tshawytscha) males representing two alternative reproductive tactics, jacks (small sneaker males) and hooknoses (large guarding males), in the presence of river water alone and OF mixed with river water. To determine the effect of genetic differences on fertilization success, we genotyped fish at neutral (microsatellites) and functional [major histocompatibility complex (MHC) II ß1] markers. We found that when sperm were competed in river water, jacks sired significantly more offspring than hooknoses; however, in OF, there was no difference in paternity between the tactics. Sperm velocity was significantly correlated with paternity success in river water, but not in ovarian fluid. Paternity success in OF, but not in river water alone, was correlated with genetic relatedness between male and female, where males that were less related to the female attained greater paternity. We found no relationship between MHC II ß1 divergence between mates and paternity success in water or OF. Our results indicate that OF can influence the outcome of sperm competition in Chinook salmon, where OF provides both male tactics with fertilization opportunities, which may in part explain what maintains both tactics in nature.     

Mating system, philopatry and patterns of kinship in the cooperatively breeding subdesert mesite Monias benschi

In the first molecular study of a member of the threatened avian family, Mesitornithidae, we used nine polymorphic microsatellite loci to elucidate parentage, patterns of within-group kinship and occurrence of extra-group paternity in the subdesert mesite Monias benschi, of southwest Madagascar. We found this cooperatively breeding species to have a very fluid mating system. There was evidence of genetic monogamy and polygynandry: of the nine groups with multiple offspring, six contained one breeding pair with unrelated helpers and three contained multiple male and female breeders with related helpers. Although patterns of within-group kinship varied, there was a strong positive relationship between group size and relatedness, suggesting that groups form by natal philopatry. There was also a strong positive correlation between within-sex and between-sex relatedness, indicating that unlike most cooperatively breeding birds, philopatry involved both sexes. In contrast to predictions of kin selection and reproductive skew models, all monogamous groups contained unrelated individuals, while two of the three polygynandrous groups were families. Moreover, although between-group variation in seasonal reproductive success was related to within-group female relatedness, relatedness among males and between the sexes had no bearing on a group's reproductive output. While kin selection may underlie helping behaviour in females, factors such as direct long-term fitness benefits of group living probably determine helping in males. Of the 14 offspring produced by fully sampled groups, at least two were sired by males from neighbouring groups: one by a breeding male and one by a nonbreeding male, suggesting that males may augment their reproductive success through extra-group paternity.     

A longitudinal analysis of reproductive skew in male rhesus macaques

One of the basic tenets of sexual selection is that male reproductive success should be large in polygynous species. Here, we analysed 6 years of molecular genetic data from a semi-free-ranging population of rhesus macaques (Macaca mulatta), using Nonac's B index, to assess the level of male reproductive skew in the study troop. On average, the top sire in each year produced 24% of the infants, while 71% of troop males sired no offspring at all. Consequently, 74% of infants had at least one paternal half-sibling in their own birth cohort. Reproductive success was greatest for high-ranking males, males who spent the whole mating season in the troop and males of 9-11 years of age. Heterozygosity for major histocompatibility complex (MHC) class II gene DQB1 was the strongest single predictor of male reproductive success. A negative relationship suggestive of female mate choice was noted between the B index and the proportion of extragroup paternities. Reproductive skew was not associated with relatedness among potential sires or with female cycle synchrony. We conclude that reproductive skew in male rhesus macaques is best accounted for by the 'limited-control' model, with multiple factors interacting to regulate individual reproductive output.     

Male genetic quality and the inequality between paternity success and fertilization success: consequences for studies of sperm competition and the evolution of polyandry

Studies of postcopulatory sexual selection typically estimate a male's fertilization success from his paternity success ( P ₂) calculated at hatching or birth. However, P ₂ may be affected by differential embryo viability, thereby confounding estimations of true fertilization success ( F ₂). This study examines the effects of variation in the ability of males to influence embryo viability upon the inequality between P ₂ and F ₂. It also investigates the consequences of this inequality for testing the hypothesis that polyandrous females accrue viability benefits for their offspring through facilitation of sperm competition (good-sperm model). Simulations of competitive mating trials show that although relative measures of male reproductive success tend to underestimate the strength of underlying good-sperm processes, good-sperm processes can be seriously overestimated using P ₂ values if males influence the viability of the embryos they sire. This study cautions the interpretation of P ₂ values as a proxy for fertilization success or sperm competitiveness in studies of postcopulatory sexual selection, and highlights that the good-sperm hypothesis needs empirical support from studies able to identify and separate unequivocally the males' ability to win fertilizations from their ability to influence the development of embryos.