Simultaneous Polyandry Research Articles

Genetic evidence for polyandry in the threatened green and golden bell frog.

Identifying which species exhibit polyandry may lead to further insights into evolutionary biology and social behaviour. However, confirming polyandry can be difficult. High-resolution genetics provides a useful means to gain evidence. Although the threatened Pelodryadid frog, the green and golden bell frog Litoria aurea, has been subject to numerous ecological studies, there is uncertainty surrounding its reproductive ecology. Polyandry has not been formally identified in L. aurea or any species within the Pelodryadidae family. We aimed to identify if there was genetic evidence of polyandry in a population occurring in a wetland complex on Kooragang Island, New South Wales. To accomplish this, we collected genetic samples of tadpoles within the same size cohort about 20-30days after explosive breeding events. Genotypes of 14 females, nine males and 70 tadpoles were analysed with COLONY (1988 single nucleotide polymorphisms after filtering) to identify parentage, full-siblings and half-siblings. We found support for the hypothesis that L. aurea is polyandrous. Based on previous observations of multi-male matings and the narrow time periods that breeding occurred in, it is likely this species exhibits simultaneous polyandry. We discuss these results in regards to behavioural adaptive processes and avenues for further research.

The Frog Fauna of Southwestern Australia: Diverse, Bizarre, Old, and Polyandrous

My research on anurans has been diverse: biogeography, speciation, acoustics, polyandry, sperm competition, and conservation. My interests in biology started in natural history but, in the late 1960s as an undergraduate student, I was receptive to emerging new ideas in biogeography and evolutionary biology: continental drift and neutral theory. My focus in this “Perspective” is an explanation of how diversity has evolved in the frog fauna of southwestern Australia, where I have worked since 1978. I discuss the roles of range fragmentation, genetic drift, directional sexual selection, polyploidy, and simultaneous polyandry as processes driving the evolution of diversity in the sometimes-bizarre frog fauna of southwestern Australia. I identify features that can characterize polyandrous anurans: e.g., large testes, sperm morphology, and, possibly, complex calls with an example of the latter in Geocrinia leai. I discuss how current anuran life histories vary across rainfall and temperature gradients and how derivation of more-arid adapted forms is a well-defined historic biogeographic pattern in southwestern Australia. My observations over time leave me cautiously optimistic about the prospects for frogs affected by global warming.

The Consequences of Polyandry for Sibship Structures, Distributions of Relationships and Relatedness, and Potential for Inbreeding in a Wild Population.

The evolutionary benefits of simultaneous polyandry (female multiple mating within a single reproductive event) remain elusive. One potential benefit could arise if polyandry alters sibship structures and consequent relationships and relatedness among females' descendants, thereby intrinsically reducing future inbreeding risk (the indirect inbreeding avoidance hypothesis). However such effects have not been quantified in naturally complex mating systems that also encompass iteroparity, overlapping generations, sequential polyandry, and polygyny. We used long-term social and genetic pedigree data from song sparrows (Melospiza melodia) to quantify cross-generational consequences of simultaneous polyandry for offspring sibship structures and distributions of relationships and relatedness among possible mates. Simultaneous polyandry decreased full sibships and increased half-sibships, on average, but such effects varied among females and were smaller than would occur in the absence of sequential polyandry or polygyny. Further, while simultaneous polyandry decreased the overall frequencies of possible matings among adult full sibs, it increased the frequencies of possible matings among adult half-sibs and more distant relatives. These results imply that the intrinsic consequences of simultaneous polyandry for inbreeding risk could cause weak indirect selection on polyandry, but the magnitude and direction of such effects will depend on complex interactions with other mating system components and the form of inbreeding depression.

Sequential polyandry through divorce and re-pairing in a cooperatively breeding bird reduces helper-offspring relatedness

Polyandry is an important component of both sexual selection and kin structuring within cooperatively breeding species. A female may have multiple partners within a single reproductive attempt (simultaneous polyandry) or across multiple broods within and/or across years (sequential polyandry). Both types of polyandry confer a range of costs and benefits to individuals and alter the genetic structure of social groups over time. To date, many molecular studies of cooperative breeders have examined the evolution of cooperative breeding in relation to simultaneous polyandry. However, cooperatively breeding vertebrates are iteroparous, and thus sequential polyandry is also likely, but more rarely considered in this context. We examined sequential polyandry in a cooperatively breeding bird that has a low level of within-brood polyandry. Over a 5-year period (2006–2010), we monitored individual mating relationships using molecular markers in a population of individually marked apostlebirds (Struthidea cinerea). Divorce occurred between reproductive seasons in 17 % (8/48) of pairs and appeared to be female-driven. The level of sequential polyandry was also driven by the disappearance of males after breeding, and over 90 % of females, for whom we had suitable data, bred with multiple males over the period of study. This sequential polyandry significantly altered the relatedness of group members to the offspring in the nest. However, in about half of the cases, the second male was related (first- or second-order relative) to the first male of a sequentially polyandrous female and this alleviated the reduction in relatedness caused by polyandry. Our findings suggest that even in species with high within-brood parentage certainty, helper-offspring relatedness values can quickly erode through sequential polyandry.

Group-spawning and Simultanous Polyandry of a Stream-dwelling Frog Feirana kangxianensis

Here we provide an example of simultaneous polyandry based on genetic evidence in Feirana kangxianensis. This stream-dwelling species occurs only in Kangxian County, southern Gansu Province, where it is sympatric with its sibling species F quadranus. During the breeding season the sex ratio of F kangxianensis was marginally female-biased (44 male:59 female) and the encounter rate in a relatively pristine habitat was significantly higher than that in heavily quarried habitats (9.6 +/- 4.8 indiv./km vs. 3.2 +/- 2.5 indiv./km). Three egg masses containing an average of 698 eggs were deposited on the underside of one or two adjacent flat rocks, 6.0-10.0 cm under the water surface and 1.0-3.5 cm above the streambed. Using Bayesian sibship clustering of nine polymorphic microsatellite genotypes, two females were detected as group-spawning in one oviposition site, with three males fertilizing each female's eggs simultaneously. We also discuss the conservation requirements of this range-restricted species and the evolutionary implication of its unusual reproductive strategy.

Sperm competitiveness differs between two frog populations with different breeding systems

In species with simultaneous polyandry, male-biased operational sex ratio is expected to increase the risk of sperm competition and thus sperm traits affecting siring success can differ among populations. Here, we test the hypothesis that high male–female ratios will enhance sperm competitiveness of Rana temporaria males. In this species, local populations can show either prolonged or explosive breeding. In a context of sperm competition and in controlled laboratory conditions, prolonged-breeding males sired a higher proportion of eggs than explosive-breeding males, regardless of female origin. This study demonstrates intrapopulation variation in siring success under a situation of sperm competition, consistent with the prolonged-explosive dichotomy of breeding strategies.

Simultaneous polyandry and heteropaternity in tiger (Panthera tigris altaica): Implications for conservation of genetic diversity in captive populations of felids

Male tigers (Panthera tigris altaica) in captivity copulate alternatively with an estrous female, suggesting a potential for heteropaternity as an effective reproductive strategy to maximize genetic diversity of offspring. We analyzed microsatellites to test and compare the genetic output of multiple male mating (simultaneous polyandry) and single male mating (monogamy) with a female in a captive population. Simultaneous polyandry resulted in heteropaternity in 66.7% observed litters. No significant differences between parental populations and between offspring populations were detected in the number of alleles (A), expected heterozygosity (H e), number of effective alleles (N e) per locus and standard individual heterozygosity (SH) (P>0.05 for all 4 indexes). Comparisons showed no significant reduction of A, H o, H e and SH from parental population to offspring population for the two mating modes (P>0.05) except for SH in polyandrous families (P=0.029). However, such reduction was equivalent to single mating families when the influence of relatedness was eliminated using effective SH (E SH ) (P>0.05). These results highlight an alternative strategy for managing captive populations of tiger and other wild felids in which animals are combined at one location allowing for copulation by multiple males to encourage heteropaternity in favor of maintained genetic diversity among offspring.

Aquatic eggs are fertilised by multiple males not engaged in amplexus in a stream-breeding frog

In anuran amphibians, multiple males amplexing a single female to fertilise her eggs has been found for less than 25 species, whereas matings without amplexus are known for less than five species. Here we provide a new example of simultaneous polyandry with multiple males not engaged in amplexus, in Feirana taihangnicus, a stream-dwelling, explosive breeder endemic to central China. Laboratory experiments showed that when one female was kept with one male in a vessel with elevated, flat stones, the female stood on her head with her swollen cloaca against the undersurface of the stone substrate to lay eggs (clutch size ranged from 371 to 533, n=7 females). Then, 10–102min after oviposition began, the male stood on his head and released sperm over the eggs distributed as a single layer on the stone surfaces. It took about 3h for the female to finish oviposition and for the male to finish fertilisation. On average, 96% of eggs were fertilised. In natural oviposition habitats, stream sections with slow flowing, we observed that 1 up to 15 males (8.7±6.6, n=6 cases), none in amplexus, participated in fertilising the eggs deposited by a single female. Evolutionary implications of this unusual reproductive strategy remain to be explored.

Evolutionary causes and consequences of sequential polyandry in anuran amphibians

Among anuran amphibians (frogs and toads), there are two types of polyandry: simultaneous polyandry, where sperm from multiple males compete to fertilize eggs, and sequential polyandry, where eggs from a single female are fertilized by multiple males in a series of temporally separate mating events, and sperm competition is absent. Here we review the occurrence of sequential polyandry in anuran amphibians, outline theoretical explanations for the evolution of this mating system and discuss potential evolutionary implications. Sequential polyandry has been reported in a limited number of anurans, but its widespread taxonomic and geographic distribution suggests it may be common. There have been no empirical studies that have explicitly investigated the evolutionary consequences of sequential polyandry in anurans, but species with this mating pattern share an array of behavioural, morphological and physiological characteristics, suggesting that there has been common sexual selection on their reproductive system. Sequential polyandry may have a number of adaptive benefits, including spreading the risk of brood failure in unpredictable environments, insuring against male infertility, or providing genetic benefits, either through good genes, intrinsic compatibility or genetic diversity effects. Anurans with sequential polyandry provide untapped opportunities for innovative research approaches that will contribute significantly to understanding anuran evolution and also, more broadly, to the development of sexual-selection and life-history theory.

Effects of simultaneous polyandry on offspring fitness in an African tree frog

In externally fertilizing animals in which females mate with multiple males at the same time (simultaneous polyandry), the possibility that females accrue genetic benefits that improve offspring viability remains largely unexamined. Here, we investigate whether simultaneous polyandry influences offspring fitness in a wild population of the Grey Foam Nest Treefrog Chiromantis xerampelina. Simultaneous polyandry in this frog is the most extreme reported for any vertebrate, with more than 90% of females mating with 10 or more males during the deposition of a single clutch. We compared growth (using age and size at metamorphosis as proxies) and survival of offspring produced by females that naturally mated with either 1 male (monandrous females) or 10‐12 males (polyandrous females). Polyandry did not influence size or age at metamorphosis, but we found that offspring from polyandrous matings had both significantly higher mean survival and reduced variance in offspring survival. These findings implicate a genetic mechanism, but targeted cross-classified breeding experiments that control for both maternal and material effects will be required to conclusively determine whether elevated offspring viability is linked to enhanced genetic diversity, intrinsic sire effects, or genetic compatibility. Irrespective of the causation, the findings provide the first evidence that naturally formed polyandrous matings have increased offspring viability in an anuran amphibian. Key words: anuran amphibian, genetic benefits, offspring viability, polyandry, sexual selection. [Behav Ecol]

Simultaneous polyandry increases fertilization success in an African foam-nesting treefrog

In many animals females mate with multiple males during a single breeding season (polyandry), but the benefits of this mating system remain poorly understood. One hypothesis is that polyandry ensures the fertilization of a female's ova (fertilization insurance hypothesis). We tested the fertilization insurance hypothesis in a natural population of African foam-nesting treefrogs, Chiromantis xerampelina, a species lacking male contest competition and in which females routinely mate with multiple males. We observed matings involving from one to 12 males and found that fertilization success was positively correlated with the number of mating males, but was unaffected by variance in clutch size or ambient temperature. Variance in fertilization success was also unrelated to the body size ratio of mating pairs. Critically, females that mated with more males also produced more tadpoles. These findings provide the first evidence that polyandry can benefit female frogs by increasing fertilization success and offspring production. We propose that fertilization insurance may account for the high incidence of simultaneous polyandry in frog species that use foam nests during breeding.

Size Dimorphism, Intrasexual Competition, and Sexual Selection in Wattled Jacana (Jacana Jacana), A Sex-Role-Reversed Shorebird in Panama

AbstractWe studied sexual size dimorphism, intrasexual competition, and sexual selection in an individually marked population of Wattled Jacanas (Jacana jacana) in the Republic of Panama. Males are the sole incubators of eggs (28-day incubation) and primary providers of chick care (50–60 days). Females were 48% heavier than, and behaviorally dominant over, males. Females also showed greater development of secondary sexual characters (fleshy facial ornamentation and wing spurs) than males. Both sexes defended territories throughout the year against same-sex conspecifics. Competition for territorial space was intense, and many individuals of both sexes did not become breeders. Resident females further competed with one another to accumulate multiple mates, resulting in a mating system of simultaneous polyandry. Female and male residents (territory holders) were larger, heavier, and more ornamented than adult floaters of the same sex. Larger and heavier females also had more mates than smaller females. Body size was thus a critical predictor of success in intrasexual competition for territories (both sexes) and for mates (females). Three measures of sexual selection—(1) sex difference in the opportunity for sexual selection, (2) female-to-male ratio of potential reproductive rates, and (3) operational sex ratio—each indicated that sexual selection is currently operating more strongly on females than on males (female-to-male ratios ranged from 1.43:1 to 2.22:1). Values of 1.61:1 and 1.43:1 represent the first published quantitative estimates of the opportunity for sexual selection for any sex-role-reversed bird. Our study supports the theory that when increased parental care entails reduced opportunities for future reproduction, asymmetries in parental care behaviors of the sexes can influence the intensity of competition for mates and the direction and strength of sexual selection.

SIZE DIMORPHISM, INTRASEXUAL COMPETITION, AND SEXUAL SELECTION IN WATTLED JACANA (JACANA JACANA), A SEX-ROLE-REVERSED SHOREBIRD IN PANAMA

Abstract We studied sexual size dimorphism, intrasexual competition, and sexual selection in an individually marked population of Wattled Jacanas (Jacana jacana) in the Republic of Panama. Males are the sole incubators of eggs (28-day incubation) and primary providers of chick care (50–60 days). Females were 48% heavier than, and behaviorally dominant over, males. Females also showed greater development of secondary sexual characters (fleshy facial ornamentation and wing spurs) than males. Both sexes defended territories throughout the year against same-sex conspecifics. Competition for territorial space was intense, and many individuals of both sexes did not become breeders. Resident females further competed with one another to accumulate multiple mates, resulting in a mating system of simultaneous polyandry. Female and male residents (territory holders) were larger, heavier, and more ornamented than adult floaters of the same sex. Larger and heavier females also had more mates than smaller females. Body...

Climatic Correlates of Breeding, Simultaneous Polyandry and Potential for Sperm Competition in the Frog Crinia georgiana

Climatic Correlates of Breeding, Simultaneous Polyandry and Potential for Sperm Competition in the Frog Crinia georgiana

Climatic Correlates of Breeding, Simultaneous Polyandry and Potential for Sperm Competition in the Frog Crinia georgiana

Specimens Examined-Phrynobatrachus alticola from Tai National Park, Ivory Coast; specimens from the middle of the park near the town of Tai: SMNS 9729 1-4, 3 males, 1 female, transects IV, V & VIII, 16.III. and 6.IV.2000; SMNS 9730 1-3, males, SRET station, IV.1999; SMNS 9731 1-2, females, transect IX, VI.2000; SMNS 9733 1-19, larvae and juveniles, IX.2000; specimen from the South of the park near the village of Guiroutou: SMNS 9732, adult female, secondary forest, 1993. Adult and juvenile P alticola from Liberian and Guinean part of Mont Nimba: MNHN 1998 1547-48, Bord de Cavally. gal. forestiere, Mt. Nimba, Guin6e, 2.1.84; MNHN 1998.2695-96, entre grassfield et New Camp ruiseau en foret, Nimba Expedition, Liberia, 27.IX.66; MNHN 1998.2655, same locality, 20.V.1969; MNHN 1998.1524, 1998.1522, 1998.1527, same locality, 18.VIII.1966; MNHN 1998.2676, same locality, 27.X.1966; MNHN 1998.1533, old Bapa Ouest, Nimba Expedition, Liberia, 21.VII.1966; MNHN 1998.2524, grassfield foret, 450 m Nimba expedition, Liberia, 20.IX.1966; MNHN 1998.2524 & 2522, Grassfield, Mt. Nimba, Liberia, 500 m, pres de la foret?, 7.VII.1966; MNHN 41 specimens without number, New Mine Road, 700m (Seka valley forest), Liberian Nimba, 4.VII.1969; MNHN 1998.2664 and 2669 and 2670, grassfield, Nimba county, Mt. Nimba, Liberia, 1.VI.1969; MNHN 1998.1197, Nimba expedition, Liberia, grassfield, foret, 29.X.1966; MNHN 1998.2643 and 2645-2647, Mt. Alpha, Nimba Liberien, 1300 m, 4.V.1969; MNHN 1998.2618-2620 and 2624, Nimba (Liberia), 550-750 m, 28.XII.1965.

Does multiple paternity improve fitness of the frog Crinia georgiana?

In the Australian myobatrachid frog Crinia georgiana simultaneous polyandry occurs in about half of all matings, which leads to multiple paternity, but reduced fertilization success and occasional female mortality. Multiple paternity may provide benefits to females that compensate for these costs, for example, through enhanced genetic diversity of a clutch. In nature, embryos and tadpoles of C. georgiana develop in shallow, temporary pools and may be exposed to fluctuating water levels and the risk of desiccation between rain events. Fertilization by genetically diverse sires may act as a bet hedge against these conditions. To evaluate this hypothesis, females were artificially mated with one or two males in the field and eggs and larvae reared in the laboratory under constant or fluctuating developmental conditions. Experiment 1 exposed embryos from single- and multiple-paternity clutches to conditions where eggs were completely covered during development or eggs sat in air on a moist substrate. Experiment 2 exposed freshly hatched larvae from single- and multiple-paternity clutches to constant wet conditions, where larvae were completely covered, or fluctuating wet conditions, where larvae ranged from being completely submersed to partially exposed over a 13-day cycle. We measured mean performance and best performance as alternate measures of genetic benefits. There were no effects of paternity on percent survival to hatching, time to hatching, body size at hatching, percent survival to metamorphosis, time to metamorphosis, or body size at metamorphosis. We also analyzed variance within clutches as a measure of genetic diversity. Again there were no predictable effects of multiple paternity. Polyandry does not appear to provide any genetic benefits that compensate for the high costs of polyandry in this species.

DOES MULTIPLE PATERNITY IMPROVE FITNESS OF THE FROG CRINIA GEORGIANA?

In the Australian myobatrachid frog Crinia georgiana simultaneous polyandry occurs in about half of all matings, which leads to multiple paternity, but reduced fertilization success and occasional female mortality. Multiple paternity may provide benefits to females that compensate for these costs, for example, through enhanced genetic diversity of a clutch. In nature, embryos and tadpoles of C. georgiana develop in shallow, temporary pools and may be exposed to fluctuating water levels and the risk of desiccation between rain events. Fertilization by genetically diverse sires may act as a bet hedge against these conditions. To evaluate this hypothesis, females were artificially mated with one or two males in the field and eggs and larvae reared in the laboratory under constant or fluctuating developmental conditions. Experiment 1 exposed embryos from single- and multiple-paternity clutches to conditions where eggs were completely covered during development or eggs sat in air on a moist substrate. Experiment 2 exposed freshly hatched larvae from single- and multiple-paternity clutches to constant wet conditions, where larvae were completely covered, or fluctuating wet conditions, where larvae ranged from being completely submersed to partially exposed over a 13- day cycle. We measured mean performance and best performance as alternate measures of genetic benefits. There were no effects of paternity on percent survival to hatching, time to hatching, body size at hatching, percent survival to metamorphosis, time to metamorphosis, or body size at metamorphosis. We also analyzed variance within clutches as a measure of genetic diversity. Again there were no predictable effects of multiple paternity. Polyandry does not appear to provide any genetic benefits that compensate for the high costs of polyandry in this species.Corresponding Editor: B. Sullivan

THE CHARACTERISTICS AND OCCURRENCE OF COOPERATIVE POLYANDRY

SummaryThis paper discusses the relative position of cooperative polyandry among models for the evolution of both polyandry and cooperative breeding. Cooperative polyandry is described as the situation where more than one male and one female breed as a group with males sharing equally in copulations and the care of one set of young. Sequential and simultaneous polyandry are defined to show how they differ from cooperative polyandry. These systems generally are characterized by the care of only one parent for each set of young, a trait which is in sharp contrast to cooperative polyandry. An argument is made that the present models for the evolution of polyandry cannot be expanded to include the cooperatively polyandrous species. Instead, the cooperative traits of cooperative polyandry fit within the array of characteristics of cooperative (communal) breeding. General characteristics of all cooperative species (monogamous, promiscuous and polyandrous) are reviewed and possible reasons for the evolution of equal‐status males are discussed. A plea is made for the unification of evolutionary models dealing with mating systems and cooperative systems.

Evolution of Polyandry in Birds

Polyandry in which one female forms either simultaneous or sequential pair bonds with more than one male is a rare vertebrate mateship system. Prior to 1972 only two cases were known with certainty among birds. All other reports of polyandry were based on inadequate information. Recently, polyandry has been demonstrated in several additional species. Surprisingly, they all belong to the avian order Charadriiformes. Comparisons of the existing polyandrous systems suggest that they can be arranged in a sequence that leads through a series of relatively minor differences from monogamy to simultaneous polyandry. Polyandrous species differ from species with other mateship systems in the following ways: females large, females more aggressive, egg or clutch size reduced, production of multiple clutches. Except in some sequential systems, the small, subordinate males perform all incubation behavior and provide all parental care for the chicks. In the Charadriiformes, polyandry has evolved in conjunction with sex role reversal and with assumption of incubation and parental behavior by the male. It is not clear why role reversal and parental behavior are related. The simplest forms of polyandry are in high-latitude birds, but the best developed forms are found in tropical species.