Multiple paternity in a philopatric rodent: the interaction of competition and choice

Paternity confusion is often suggested as the benefit that femalemammals accrue by mating with multiple males, but genetic advantagesare also possible. Microsatellite-based parentage analyses demonstratethat female banner-tailed kangaroo rats (Dipodomys spectabilis)commonly mate with more than one male; we asked how male andfemale behaviors interact to influence the characteristics ofmales that sire offspring. Specifically, we compared attributes(age, weight, mobility, relatedness, proximity) of the fathersof 229 known-maternity offspring with those of the other malesaccessible to the mothers. Adult males living adjacent to eachfemale attempt to monopolize access to her, and the nearestmale sires a plurality of offspring, but most mothers' youngare fathered by more than one male and littermates are usuallyhalf-sibs. Male proximity and mobility, but not size, influencethe probability of paternity, suggesting a role for competitivemate searching. Females significantly reduce the inbreedingcoefficient of their offspring by mating with males other than(or in addition to) the nearest male. Fathers are less closelyrelated to the mother in years of high density when unrelatedmales are more accessible to the female. Our results favor thegenetic "bet-hedging" hypothesis, whereby females actively butunselectively seek matings with additional males when the malemost likely to win in mate competition is costly to her (inthis case, genetically less compatible). We anticipate thatgenetic bet hedging will be common in species whose femalesare defendable, especially if they are also philopatric.     

Responses of territorial and floater male Red‐winged Blackbirds to models of receptive females

Red‐winged Blackbirds (RWBL; Agelaius phoeniceus) have a polygynous mating system and, because territorial males commonly have harems of two to five females, some second‐year (SY) and after‐second‐year (ASY) males do not establish nesting territories, but become floaters. Previous studies have revealed high rates of extra‐pair copulations in this species and that sexually mature male floaters and territory owners do not differ in size, testosterone levels, or reproductive capability, suggesting that floaters may occasionally gain paternity. During May and June 2008, we observed the behavioral responses of floater males to taxidermic mounts (models) of female RWBL placed in a precopulatory position. Floaters intruded into territories during 46% of model presentations, with 20% of intrusions by ASY floaters and 80% by SY floaters. During intrusions, ASY floaters attempted to copulate with models 93% of the time compared to 80% for SY floaters. Copulations were successful during 30% of attempts by ASY males and 25% of attempts by SY floaters. The frequency of intrusions by ASY and SY floaters, attempted copulations by SY floaters, and successful copulations by ASY floaters increased as territorial males spent more time off their territories. Responses of floater males toward models in our study suggest that floater male RWBL attempt to exploit available breeding opportunities. The lack of evidence for extrapair young (EPY) fathered by floater male RWBL in previous studies, combined with our results indicating that the presence of territorial males limits floater intrusions, copulation attempts, and successful copulations, suggests that the reproductive success of floater males is limited in part by the aggressive behavior of territorial males.     

Effects of age and experience on the responses of territorial and floater male Red‐winged Blackbirds to models of receptive females

The ability of sexually mature non‐territorial floaters to sire offspring affects the success of floating as a breeding strategy. Red‐winged Blackbirds (Agelaius phoeniceus) have second‐year (SY) and after‐second‐year (ASY) floater males, and genetic studies suggest that floaters may gain paternity. Despite these studies, we still know little about the fitness costs and benefits of floating in this species. By presenting taxidermic models of females in soliciting, precopulatory postures in territories of experienced (previously attracted at least one mate in the study area) and inexperienced (did not previously defend a territory in the study area) males, I was able to examine the copulation behavior and success of floater male Red‐winged Blackbirds as well as the effect of experience for territorial males. Floaters trespassed during 66.1% of presentations and 85.4% of trespassers were SY males. Experienced territorial males (92.5%) and neighbors (87.5%) were most successful in attempts to copulate with models, inexperienced territorial males (62.5%) and ASY floaters (50.0%) had intermediate success, and SY floaters (6.9%) were least successful. Experienced territorial males were more likely to approach models than inexperienced males, and floaters were more likely to approach models in territories of experienced than inexperienced males. These results provide further evidence that floaters trespass frequently, suggest that floaters sire offspring, and demonstrate that prior breeding experience affects the behavior and reproductive success of territorial male Red‐winged Blackbirds. Floating appears to be a conditional strategy for ASY male Red‐winged Blackbirds, but, because it is still not known if SY floaters sire offspring, these males may be trespassing to gain information or experience.     

The direction of mothers' and daughters' preferences and the heritability of male ornaments in red jungle fowl (Gallus gallus)

We used a breeding design involving 18 sires and 108 dams tostudy the heritabilities of male ornaments in red jungle fowl(Gallus gallus). Ornaments used by females to choose mates showedlow heritabilities, with the exception of comb and wattle measures.The general absence of heritability suggests that a geneticcovariance did not exist at the time of this study between mostmale ornaments and female preferences for those ornaments. Thisresult is contrary to a key prediction of the arbitrary or Fisherianhypothesis of sexual selection. Comb size and color are condition-dependenttraits that reflect short-term changes in health, and comb sizeof males was positively correlated with offspring weight. Ourresults are consistent with the expectation of good-genes hypothesesthat male ornaments reflect the ability of males to withstandenvironmental stresses.     

Caribbean damselfish with varying territory quality: correlated behaviors but not a syndrome

The behavioral syndrome hypothesis suggests that individualanimals within a population behave differently due to specificbehavioral types, and these should be consistent across behaviorsor in different contexts. In contrast, for animals that livewithin an environment in which territory quality can changeover time, natural selection should have favored behavioralflexibility and modulation of the cost of defense in relationto territory quality. This would require assessment of the territoryfollowed by displays of appropriate types and intensities ofbehavior. We examined the territorial behavior of male beaugregorydamselfish (Stegastes leucostictus) by enhancing territory qualityusing artificial breeding sites and comparing their behaviorto males on lower quality natural sites. When male fish weredefending high-quality artificial territories, they had higherlevels of aggression toward male conspecifics and courtshiptoward females than when on low-quality natural territories.We also found that aggression and courtship behaviors were correlatedon natural sites but not on artificial sites. Behaviors werenot correlated within individuals when males switched from naturalto artificial territories or from artificial to natural territories.These results indicate that males assess their current territoriesand adjust behaviors accordingly and that courtship and aggressivebehaviors are not linked within a permanent behavioral syndrome.     

Genetic analysis of the mating system and opportunity for sexual selection in northern water snakes (Nerodia sipedon)

We used data collected over 3 years at two study sites to quantifythe rates and consequences of multiple paternity and to determinethe opportunity for selection on male and female northern watersnakes (Nerodia sipedon). We sampled litters from 45 femalesthat gave birth to 811 offspring. Using eight microsatelliteDNA loci (probability of exclusion of nonparental males >0.99), we assigned paternity to 93% of neonates from one studypopulation and 69% of neonates from the other population. Observationsof participation in mating aggregations predicted individual reproductive success poorly for two reasons. First, males regularlycourted nonreproductive females. Second, more than half ofall sexually mature males obtained no reproductive successeach year, despite the fact that many of them participatedin mating aggregations. The number of sires per litter ranged from one to five, with 58% of all litters sired by more thanone male. Multiple paternity increased with female size, apparentlyboth because bigger females mated with more males and becausethe larger litters of big females provide paternity opportunitiesto more males. Multiple paternity was also more prevalent inyears with shorter mating seasons. We detected no advantage to multiple paternity in reducing either the number of unfertilizedovules or stillborn young. Despite the majority of males siringno young each year, some males fathered young with as manyas three different females in one year. Male reproductive successincreased by more than 10 offspring for each additional mate,whereas female success increased by fewer than 2 offspring foreach additional mate. The opportunity for sexual selectionwas more than five times higher in males than females.     

Arctic charr strain crosses: effects on growth and sexual maturity

Three Arctic charr strains and their crosses were evaluated with respect to growth and sexual maturation frequency. No significant heterosis was observed for growth. One out of five crosses was heavier, but not significantly so, than the best performing parental strain at ages 1 + and 2. The five other crosses did not perform better than the best performing parental strain at any age. Cross-breeding was not recommended as an effective method to improve growth performance in Arctic charr. Growth performance of reciprocal crosses differed significantly in all strain combinations: crosses resembled more the male parent strain than the female parent strain. ANOVA for male maturation frequency showed a highly significant effect of the male parent strain and a weakly significant effect of female parent strain. In the Ottsjö strain mature males were significantly larger than immature fish and females. Such size difference was also observed in the offspring when sires of the Ottsjö strain were crossed with dams of the faster growing Honavan strain or with dams of the Rensjö strain. When Ottsjö dams were crossed to sires of the other strains no significant size difference between mature males and other fish was found.     

Multiple mating and reproductive skew in Trinidadian guppies

Male offspring production in promiscuously mating species is typically more skewed than female offspring production. It is therefore advantageous for males to seek as many mating partners as possible. However, given the documented benefits of polyandry we expect females, as well as males, to mate multiply. We tested these ideas using Trinidadian guppies, Poecilia reticulata. Fishes were collected from the wild, housed in groups of 10 males and 10 females and allowed to reproduce freely over a period of three months. We used hypervariable microsatellite loci to identify the parents of 840 offspring and to quantify the variance in mating success. As anticipated, and in line with the Bateman gradient, there was greater skew in the number of progeny produced by males. By contrast, we found no sex difference in mating partner number over the duration of the experiment. A median of two males fathered each brood and there was marked turnover in the identities of the sires of successive broods. Female partner turnover was, however, less than expected under random mating. We suggest that partner switching over time, as well as polyandry within broods, could contribute to the maintenance of genetic diversity in guppy populations.     

Correlates of reproductive success within alternative mating tactics of the common shrew

Male common shrews (Sorex araneus) adopt two discrete matingtactics. The most successful males, in terms of number of offspringfathered, are those that establish large overlapping home rangesin areas of high female density early in the breeding season.An alternative, less successful mating tactic is to travel longdistances in search of mating opportunities. This study is aninvestigation of correlates of reproductive success for malesadopting these different mating tactics. Reproductive successunder natural conditions was assessed using DNA fingerprinting,and survival of offspring was monitored in the field. The numberof offspring fathered by males with overlapping home rangeswas positively correlated with the number of female ranges overlappedduring the breeding season and with testes mass. The numberof offspring fathered by males that made long-distance movementswas positively correlated with their epididymal sperm counts.It is argued that competitively superior (overlapping) malesachieve high reproductive success by competing to maximize thenumber of females inseminated, whereas those adopting an alternativemating tactic instead compete largely via sperm competition,aiming to maximize insemination success with any particularfemale. There was no significant difference in the fluctuatingasymmetry (FA) of males adopting different mating tactics (FAwas measured as the difference in length of the paired lateralscent glands). Fluctuating asymmetry was not related to thenumber of offspring fathered by males adopting either matingtactic, but was significantly correlated with the proportionof male offspring fathered that survived to sexual maturity.Although apparently not correlated with mating success in thisspecies, FA may reflect some aspect of genetic quality thataffects offspring survival. [Behav Ecol 7: 334–340 (1996)]     

Reconstruction of Parentage in a Band of Captive Hamadryas Baboons

The male leaders of free-ranging harem groups of hamadryas baboons are believed to mate exclusively with the female members of their harems, which typically contain no more than 2–3 females. Using no-parent parentage exclusion analysis (PEA) we identified the paternity of 25 offspring born in a captive band of hamadryas baboons (Papio hamadryas hamadryas) containing five adult males, each with a stable harem of about five females. Nine of 13 microsatellite (SSR) loci known to be highly polymorphic in rhesus macaques (Macaca mulatta) were successful in identifying the sires of all but two offspring without knowledge of the dams' genotypes, and we were able to determine the sires of all offspring when the dams' genotypes were considered. Mating success of the males ranged between 2 and 7 offspring and bore no clear relationship to the males' ages, ranks or the number of females in their harems. The males sired 7 of the 25 offspring with females outside their own harems, with higher-ranking males exhibiting greater success monopolizing access to females in their harem than lower-ranking males did. More surprisingly, the females assigned as the dams of 14 of the 25 offspring could be unequivocally excluded from parentage. The identity of the true dam could be determined for each of these 14 offspring using single-parent PEA and was uncorrelated with the ranks of these offsprings' sires and whether the offspring were born to dams outside the sires' harem groups. The combined effect of this extraharem mating and kidnapping was that only 12 of the 25 offspring were raised within their sires' harem groups. A second group of hamadryas baboons of identical structure exhibited the same high incidences of infant kidnapping and mating outside the harem group. It is unclear whether these behaviors provide an adaptive advantage or represent aberrant behavior resulting from captivity or other circumstances.     

Role-Reversed Nepotism Among Cubs and Sires in the Spotted Hyena (Crocuta crocuta)

Nepotism is widespread among parents and offspring, and is typically associated with fundamental asymmetries; parents can usually do more to help their offspring than vice versa, and the cost of a given nepotistic behavior is usually less for parents than for offspring. This may not be so among spotted hyenas (Crocuta crocuta); sires never achieve social rank equal to that of their cubs, to whom they provide no obvious paternal care. Nepotism by sires towards their cubs is thus socially constrained. However, the higher social status of cubs might offset cubs’ developmental disadvantages and permit nepotistic treatment of sires by offspring. We therefore sought to determine whether the interactions among spotted hyena cubs and adult males were influenced by kinship, using long‐term observations from one clan of spotted hyenas. Sires exhibited no overt nepotism towards their cubs in most behaviors, but they did associate more closely with their daughters than with unrelated control females. Sires also associated more closely with their daughters than with their sons, with whom they associated no more closely than they did with unrelated control males. Cubs favored their sires by directing less intense aggression towards them than towards unrelated control males. Cubs of both sexes also associated more closely with their sires than with control males after the cubs were independent of the clan's communal den. Although sires evidently recognize their offspring, paternal nepotism by sires towards their cubs is weaker than filial nepotism by cubs towards their sires. The small size and immaturity of cubs thus appear to be weaker constraints on nepotism than is the low social status of their sires.     

SEXUAL SELECTION IN AMERICAN TOADS: A TEST OF A GOOD-GENES HYPOTHESIS

Adaptive mate choice in species lacking male resource control and/or paternal care might be maintained by selection because preferred males sire genetically superior offspring. For such a process to occur, some male phenotypic trait(s) must both reliably indicate male genetic quality and influence the pattern of mate choice by females. In American toads, Bufo americanus, male body length has been documented to influence female mating patterns: females usually mate with males that are larger than average. However, the relationship between male size and male genetic quality is unknown. We conducted a controlled breeding experiment using 48 sires and 19 dams to determine if larger males sire offspring with superior larval performance characteristics (greater survival to metamorphosis, larger mass at metamorphosis, and earlier metamorphosis). We also aged each sire to test the hypothesis that older males are, on average, genetically superior to younger males. We crossed each female with three sires representing three body size categories (mean and 1 SD ± mean snout-ischium length). Hatchlings (500 from each cross) were reared to metamorphosis in seminatural ponds in the field. Metamorph weight (log transformed) and age at metamorphosis showed significant heritability and were genetically correlated with each other. Hence, sires differed in genetic quality. However, none of the three measures of offspring performance was correlated with sire body size or age. Thus, we obtained no support for the prediction that sire body size or age is related to genetic quality.     

Consistent individual variations in aggressiveness and a behavioral syndrome across breeding contexts in different environments in the Black-tailed Gull

Individual behaviors of animals do not evolve separately; they do so in association with other behaviors caused by single shared genetic or physiological constraints and/or favored by selection. Thus, measuring behavioral syndromes—suites of correlated behaviors across different contexts—leads to a better understanding of the adaptive significance of variations in behaviors. However, relatively few studies have examined behavioral syndromes in wild animal populations in changing environments. We investigated a potential behavioral syndrome across antipredator nest defense, territorial defense, chick provisioning, and mating behaviors of male Black-tailed Gulls Larus crassirostris in two successive years under different conspecific territorial intrusion risks and food conditions. Males that presented high levels of antipredator nest defense (aggressive antipredator defenders) against a crow decoy (crows are egg predators) defended their territories against conspecific intruders more frequently than did other males (nonaggressive antipredator defenders), independent of the risk of intrusion. Aggressive antipredator defenders also fed their chicks more frequently than nonaggressive males, but only in a year of low food availability. Taken together, this indicates that males show consistent aggressiveness regardless of breeding context (antipredator and territorial defense), but can regulate food provisioning according to food availability.     

Social mating system and reproductive success in house wrens

Current models explaining the establishment and maintenanceof social monogamy and polygyny within avian populations typicallyassume that the reproductive success of polygynous males exceedsthat of monogamous males. This assumption is almost always supportedwhen the number of fledglings or recruits to future breedingpopulations is used to measure adult reproductive success. However,recent studies using DNA markers indicate that simple countsof fledglings or recruits may be a poor estimator of the numberof nestlings sired by the social father. In this paper, we comparethe number of genetic offspring produced by socially monogamousand polygynous house wren (TrogiodyUs atdon) males in nestsat which they were the social father. Polygynous males did,in fact, sire more nestlings in their own nests than did monogamousmales. Moreover, although we have not identified the sires ofextrapair nestlings, we document that even when all extrapairnestlings in this population are hypotheticaOy assigned to monogamousmales, die total reproductive success of polygynous males exceedsthat of monogamous males. These results and those of severalother recent studies are consistent with the assumption thatpolygynous males produce more offspring than monogamous males.     

Paternal reproductive strategy influences metabolic capacities and muscle development of Atlantic salmon (Salmo salar L.) embryos

Male Atlantic salmon follow a conditional strategy, becoming either "combatants" that undertake a seaward migration and spend at least a year at sea or "sneakers" that remain in freshwater and mature as parr. A variety of physiological indices showed significant but small differences between the offspring of males that use these two reproductive tactics. Offspring fathered by anadromous male Atlantic salmon (Salmo salar L.) showed greater muscular development and muscle metabolic capacities but lower spontaneous movements than those fathered by mature male parr. At hatch and at maximum attainable wet weight (MAWW), offspring fathered by anadromous males had higher activities of mitochondrial (cytochrome C oxidase and citrate synthase) and glycolytic (lactate dehydrogenase [LDH]) enzymes than progeny of mature male parr. Enzymatic profiles of progeny of anadromous fathers also suggested greater nitrogen excretion capacity (glutamate dehydrogenase) and increased muscular development (creatine kinase and LDH) than in the progeny of mature parr. At MAWW, juveniles fathered by mature parr made considerably more spontaneous movements, presumably increasing their energy expenditures. For juveniles fathered by anadromous males, total cross-sectional areas of white and red muscle at hatch were higher due to the greater number of large-diameter fibers. We suggest that the slightly lower metabolic capacities and muscular development of alevins fathered by mature parr could reflect differences in energy partitioning during their dependence on vitellus. Greater spontaneous movements of offspring of mature male parr could favor feeding and growth after the resorption of the vitellus.     

Male reproductive strategy and the importance of maternal status in the Antarctic fur seal Arctocephalus gazella

Abstract. Although mammalian mating systems are classically characterized in terms of male competition and polygyny, it is becoming increasingly apparent that alternative male strategies and female choice may play important roles. For example, females who mate with males from a dominant dynasty risk producing inbred offspring. Many pinnipeds are highly polygynous, but in some species alternative male strategies such as aquatic mating appear to be important, even when behavioral observations suggest strong polygyny. Here, we analyze male reproductive success in the Antarctic fur seal Arctocephalus gazella , an otariid described behaviorally as being highly polygynous, by combining a microsatellite paternity analysis spanning seven consecutive breeding seasons with detailed behavioral data on both sexes. Territorial males fathered 59% of 660 pups analyzed from our study colony. Male reproductive skew was considerable, with a quarter of all paternities assigned to just 12 top individuals on a beach where mean annual pup production was 635. Most males were successful for only a single season, but those able to return over successive years enjoyed rapidly increasing success with each additional season of tenure. We found no evidence of alternative male reproductive tactics such as aquatic or sneaky terrestrial mating. However, paternity was strongly influenced by maternal status. Females observed on the beach without a pup were significantly less likely to conceive to a sampled territorial male than equivalent females that did pup. In addition, their pups carried combinations of paternal alleles that were less likely to be found on the study beach and exhibited lower levels of shared paternity. Thus, from a territorial male's perspective, not all females offer equal opportunities for fertilization.     

No evidence for a genetic association between female mating preference and male secondary sexual trait in a Lake Victoria cichlid fish

Sexual selection by female mating preference for male nuptial coloration has been suggested as a driving force in the rapid speciation of Lake Victoria cichlid fish. This process could have been facilitated or accelerated by genetic associations between female preference loci and male coloration loci. Preferences, as well as coloration, are heritable traits and are probably determined by more than one gene. However, little is known about potential genetic associations between these traits. In turbid water, we found a population that is variable in male nuptial coloration from blue to yellow to red. Males at the extreme ends of the phenotype distribution resemble a reproductively isolated species pair in clear water that has diverged into one species with blue-grey males and one species with bright red males. Females of the turbid water population vary in mating preference coinciding with the male phenotype distribution. For the current study, these females were mated to blue males. We measured the coloration of the sires and male offspring. Parents-offspring regression showed that the sires did not affect male offspring coloration, which confirms earlier findings that the blue species breeds true. In contrast, male offspring coloration was determined by the identity of the dams, which suggests that there is heritable variation in male color genes between females. However, we found that mating preferences of the dams were not correlated with male offspring coloration. Thus, there is no evidence for strong genetic linkage between mating preference and the preferred trait in this population [Current Zoology 56 (1): 57-64 2010].     

Polyandry and fitness of offspring reared under varying nutritional stress in decorated crickets

Abstract.— Females, by mating with more than one male in their lifetime, may reduce their risk of receiving sperm from genetically incompatible sires or increase their prospects of obtaining sperm from genetically superior sires. Although there is evidence of both kinds of genetic benefits in crickets, their relative importance remains unclear, and the extent to which experimentally manipulated levels of polyandry in the laboratory correspond to those that occur in nature remain unknown. We measured lifetime polyandry of free-living female decorated crickets, Gryllodes sigillatus , and conducted an experiment to determine whether polyandry leads to an increase in offspring viability. We experimentally manipulated both the levels of polyandry and opportunities for females to select among males, randomly allocating the offspring of experimental females to high-food-stress or low-food-stress regimes to complete their development. Females exhibited a high degree of polyandry, mating on average with more than seven different males during their lifetime and up to as many as 15. Polyandry had no effect on either the developmental time or survival of offspring. However, polyandrous females produced significantly heavier sons than those of monandrous females, although there was no difference in the adult mass of daughters. There was no significant interaction between mating treatment and offspring nutritional regimen in their effects on offspring mass, suggesting that benefits accruing to female polyandry are independent of the environment in which offspring develop. The sex difference in the extent to which male and female offspring benefit via their mother's polyandry may reflect possible differences in the fitness returns from sons and daughters. The larger mass gain shown by sons of polyandrous females probably leads to their increased reproductive success, either because of their increased success in sperm competition or because of their increased life span.     

Comprehensive paternity assignment: genotype,spatial location and social status in song sparrows,Melospiza Melodia

Comprehensive, accurate paternity assignment is critical to answering numerous questions in evolutionary ecology. Yet, most studies of species with extra‐pair paternity (EPP) fail to assign sires to all offspring. Common limitations include incomplete and biased sampling of offspring and males, particularly with respect to male location and social status, potentially biasing estimated patterns of paternity. Studies that achieve comprehensive sampling and paternity assignment are therefore required. Accordingly, we genotyped virtually all males and >99% of 6‐day‐old offspring over 16 years in a song sparrow (Melospiza melodia) population and used three complementary statistical methodologies to attempt complete paternity assignment for all 2207 offspring. Assignments were highly consistent across maximum likelihood methods that used solely genotype data, and heuristic and integrated Bayesian analyses that included data describing individual locations. Sires were assigned to >99% of all genotyped offspring with ≥95% confidence, revealing an EPP rate of c. 28%. Extra‐pair sires primarily occupied territories neighbouring their extra‐pair offspring; spatial location was therefore highly informative for paternity assignment. EPP was biased towards paired territorial males, although unpaired territorial and floater males sired c. 13% of extra‐pair offspring. Failing to sample and include unpaired males as candidate sires would therefore substantially reduce assignment rates. These analyses demonstrate the integration of genetic and ecological information to achieve comprehensive paternity assignment and direct biological insight, illustrate the potential biases that common forms of incomplete sampling could have on estimated patterns of EPP, and provide an essential basis for understanding the evolutionary causes and consequences of EPP.