Female polyandry affects their sons’ reproductive success in the red flour beetle Tribolium castaneum

A potential benefit to females mating with multiple males is the increased probability that their sons will inherit traits enhancing their pre‐ or post‐mating ability to obtain fertilizations. We allowed red flour beetle (Tribolium castaneum) females to mate on three consecutive days either repeatedly to the same male or to three different males. This procedure was carried out in 20 replicate lines, 10 established with wild‐type, and 10 with the Chicago black morph, a partially dominant phenotypic marker. The paternity achieved by the sons of females from polyandrous vs. monandrous lines of contrasting morph was assessed in the F1, F2 and F3 generation by mating wild‐type stock females to two experimental males and assigning the progeny to either sire based on phenotype. The sons of polyandrous wild‐type females achieved significantly higher paternity when mating in the second male role than the sons of monandrous wild‐type females. By contrast, when mating in the first male role, males produced by females from polyandrous lines tended to have lower paternity than males from monandrous lines. Both effects were independent of the number of mates of the black competitor’s mother, and interacted significantly with the number of progeny laid by the female. These results provide the first evidence that manipulating the number of mates of a female can influence her sons’ mating success and suggest a potential trade‐off between offence and defence in this species.     

Females benefit from multiple mating but not multiple mates in the burying beetle Nicrophorus vespilloides

Male reproductive success generally increases with number of mates but this need not be true for females. If females are the limiting sex, as few as one mate can be optimal. Despite the theoretical differences driving multiple mating in the sexes, multiple mating is the norm rather than the exception. Empirical investigations are therefore required to determine why females mate with multiple males. Both nonadaptive (correlated responses to selection on males, given the mean mating rates have to be the same) and adaptive (direct or indirect fitness benefits) can drive the evolution of multiple mating in females. Females of the burying beetle Nicorphorus vespilloides often mate repeatedly with the same male, but this appears to be a correlated response to selection on males rather than reflecting direct benefits to females for multiple mating. However, an unexamined alternative to this nonadaptive explanation is that females benefit by mating with multiple different males and therefore are selected for general promiscuity. Here we examine if mating polyandrously provides fitness benefits by examing the effects of number of mates (1, 2 or 3), mating system (monogamous, polyandrous) and their interaction. The only significant influence was mating more than once. This did not depend on type of mating. We suggest that unlike most other species examined, in N. vespilloides mating with the same male repeatedly or with several different males reflects an indiscriminate willingness to mate as a result of correlated selection on males for high rates of mating.     

Female mating decisions: maximizing fitness?

Sexual selection theory assumes that maximizing fitness is the ultimate goal in every mating decision. Fitness can be maximized directly by increasing the number of offspring (direct benefits) or indirectly by maximizing offspring's lifetime reproductive success (indirect benefits). Whereas there is considerable evidence in the literature for the influence of mating decisions on direct benefits, indirect benefits have been more elusive. Here, we review the variables that influence mating decisions made by females of freshwater fish and how these affect their fitness directly, as well as indirectly. Females enhance their fitness by matching their mating decisions to current environmental conditions, using a wide range of pre- and post-copulation mechanisms that enable them to maximize benefits from mating. Male sexual traits and courtship displays are signals used by females as a way of assessing male quality in terms of both direct and indirect benefits. Polyandry is very common among freshwater fish species, and indirect benefits have been hypothesized as drivers of its predominance. Despite intensive theoretical work, and multiple suggestions of the effects of indirect benefits, to date no study has been able to demonstrate experimentally the existence of indirect benefits in freshwater fish species. Additionally, most studies of direct benefits measure short-term benefits of mating decisions. In both cases, lifetime reproductive success is not assessed. Therefore, we are led to conclude that evidence as to whether female mating decisions result in direct and/or indirect benefits in freshwater fish species is still lacking. These results should be considered in light of the ongoing debate about the significance of indirect benefits in female mating decisions.     

Asynchronous arrival pattern, operational sex ratio and occurrence of multiple paternities in a territorial breeding anuran, Rana dalmatina

Understanding why females mate multiply is a major issue in evolutionary ecology. We investigated the consequences of an asynchronous arrival pattern on male competition and multiple paternity in the apparently monoandrous agile frog ( Rana dalmatina ). The largest frogs arrived first and both males and females lost weight significantly during the spawning period. Asynchronous arrival at breeding sites resulted in a male-biased operational sex ratio (OSR). The OSR was more strongly male-biased at the beginning and at the end of the breeding period when the number of satellite males increased. All females mated only once, but multiple paternity within clutches occurred at the beginning and the end of the breeding period. The influence of asynchronous arrival and biased sex ratio suggests that reduced variance or bet-hedging promoting female fitness had only a reduced role in the evolution of polyandry, and polyandry is likely to be associated with male benefits. Polyandry in frogs can be explained either by forced mating as a result of sexual conflict or by clutch piracy. By modifying intrasexual competition, asynchronous arrival and changes in OSR may have a decisive influence upon the evolution of mating systems and favour both polyandry and stable coexistence of alternative mating behaviour.  © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 86 , 191–200.     

Evidence of Monandry in a Mosquito (<Emphasis Type="Italic">Sabethes cyaneus</Emphasis>) with Elaborate Ornaments in Both Sexes

Despite the benefits of multiple mating to females many mosquitoes appear to be monandrous. Members of the mosquito tribe Sabethini are unique among the mosquitoes for they possess iridescent scales and elaborate ornaments in both sexes. Additionally, this tribe boasts the only reported cases of courtship display within the mosquitoes. Due to these singular traits and behaviors, we predicted that members of this tribe have a different mating system with relatively high female mating rate. We tested this prediction in the ornamented mosquito Sabethes cyaneus. Contrary to our prediction, however, females were monandrous throughout their lifetime and multiple gonotrophic cycles. We discuss the possible implications of monandry on the evolution of sexually homologous ornaments, with particular consideration of mutual mate choice.     

Sperm competition and the significance of female multiple mating in the predatory mite Parasitus fimetorum

Females of the predatory mite Parasitus fimetorum (Gamasida; Parasitina) inhabiting animal manure indiscriminately copulate with many mates. The sperm competition between the males was estimated by electrophoresis of allozymes and the effects of multiple mating on female reproduction were investigated. When females were forced to mate only once, their fecundity decreased drastically compared to the case of multiple mating (but longevity was unaffected). When one female mated with two males, the outcome of sperm competition depended greatly upon the mating interval. When the second mating occurred immediately after the first, the female fecundity decreased as in the case of single mating and the second male fertilized only a few eggs. However, when there was an interval of 1 day between the two matings, the females achieved normal fecundity and the second male fertilized approximately half the eggs. This suggests that the spermatophore deposited by the first male may act as a short-term copulatory plug in the female's genital opening. When one female mated with several males with 1 day intervals, three or more males shared fertilization of the eggs. This study suggests that the multiple mating of females is a necessary stimulus to continue oogenesis and some physiological factors for this stimulation may exist in spermatophores.     

Extreme sequential polyandry insures against nest failure in a frog

Sequential polyandry may evolve as an insurance mechanism to reduce the risk of choosing a mate that is infertile, closely related, genetically inferior or incompatible, but polyandry also might insure against nest failure in unpredictable environments. Most animals are oviparous, and in species where males provide nest sites whose quality varies substantially and unpredictably, polyandrous females might insure offspring success by distributing their eggs across multiple nests. Here, we test this hypothesis in a wild population of an Australian terrestrial toadlet, a polyandrous species, where males construct nests and remain with broods. We found that females partitioned their eggs across the nests of two to eight males and that more polyandrous females gained a significant increase in mean offspring survivorship. Our results provide evidence for the most extreme case of sequential polyandry yet discovered in a vertebrate and also suggest that insurance against nest failure might favour the evolution of polyandry. We propose that insurance against nest failure might be widespread among oviparous taxa and provide an important explanation for the prevalence of sequential polyandry in nature.     

POLYGYNANDRY IN THE DUSKY PIPEFISH SYNGNATHUS FLORIDAE REVEALED BY MICROSATELLITE DNA MARKERS

In the dusky pipefish Syngnathus floridae, like other species in the family Syngnathidae, ‘pregnant’ males provide all post-zygotic care. Male pregnancy has interesting implications for sexual selection theory and the evolution of mating systems. Here, we employ microsatellite markers to describe the genetic mating system of S. floridae, compare the outcome with a previous report of genetic polyandry for the Gulf pipefish S. scovelli, and consider possible associations between the mating system and degree of sexual dimorphism in these species. Twenty-two pregnant male dusky pipefish from one locale in the northern Gulf of Mexico were analyzed genetically, together with subsamples of 42 embryos from each male's brood pouch. Adult females also were assayed. The genotypes observed in these samples document that cuckoldry by males did not occur; males often receive eggs from multiple females during the course of a pregnancy (six males had one mate each, 13 had two mates, and three had three mates); embryos from different females are segregated spatially within a male's brood pouch; and a female's clutch of eggs often is divided among more than one male. Thus, the genetic mating system of the dusky pipefish is best described as polygynandrous. The genetic results for S. floridae and S. scovelli are consistent with a simple model of sexual selection which predicts that for sex role-reversed organisms, species with greater degrees of sexual dimorphism are more highly polyandrous.     

Mating Behavior of Southern Stingrays, Dasyatis americana (Dasyatidae)

We document in detail the first complete sequence of mating events in the southern stingray, Dasyatis americana, based on observations of four matings (five separate copulations) at Grand Cayman, British West Indies and Bimini, Bahamas. These observations are significant because almost nothing is known about this important aspect of the life cycle of batoids, due to the rarity of encounters with mating animals in natural settings. Similar to mating behavior described in the manta ray, Manta birostris, the mating sequence of D. americana can be characterized as (1) 'close-following', (2) 'pre-copulatory biting', (3) 'insertion/copulation', (4) 'resting' and (5) 'separation'. Additional information gained from these observations includes the fact that (1) two of the females were mated very shortly (i.e. within minutes–hours) after parturition and (2) one of the mating events involved a single female that copulated (unforced) with two males in rapid succession. The latter observation suggests that polyandry and multiple paternity may be elements of the mating system of D. americana.     

Mating rate and fitness in female bean weevils

Females of most animal taxa mate with several males during theirlifespan. Yet our understanding of the ultimate causes of polyandryis incomplete. For example, it is not clear if and in what sensefemale mating rates are optimal. Most female insects are thoughtto maximize their fitness by mating at an intermediate rate,but it has been suggested that two alternative fitness peaksmay be observed if multiple costs and benefits interact in determiningthe relationship between mating rate and fitness. We studiedthe relationship between female fitness and mating rate in thebean weevil, Callosobruchus maculatus (Coleoptera: Bruchidae),a species in which several distinct direct effects of matingto females have been reported. Our results show that femalefitness, measured as lifetime offspring production, is lowestat an intermediate mating rate. We suggest that this patternis the result of multiple direct benefits to mating (e.g., spermreplenishment and hydration/nutrition effects) in combinationwith significant direct costs to mating (e.g., injury from malegenitalia). Females mating at low rates may efficiently minimizethe costs of mating, whereas females mating at high rates insteadmay maximize the benefits of mating. If common, the existenceof bimodal relationships between female mating rate and fitnessmay help explain the large intra- and interspecific variationin the degree of polyandry often seen in insects.