Paternal effort related to experimentally manipulated paternity of male collared flycatchers

The way that variation in paternity affects the optimal level of paternal effort has been a contentious issue, both in terms of theory and the empirical data needed to test competing theories. Clarification of the theoretical issues has led to the prediction that a reduction in paternal effort should only be expected when (i) there are substantial costs of paternal care and (ii) males have available some cue to their share of paternity in the current brood. Previous work on the collared flycatcher, Ficedula albicollis, has shown that the first condition is supported because of trade-offs between paternal effort and secondary sexual character size. We carried out experimental manipulations of pairs of collared flycatchers (temporary male removal), which were effective in causing variation in paternity in the current brood. Male responses to these manipulations were studied by quantifying levels of paternal care. All males reared nestlings cross-fostered from non-experimental nests at the egg stage, thus ruling out the possibility that they responded to direct cues about paternity. The timing of male removal predicted the male''s share of paternity, suggesting that males had a clear cue to their share of paternity, thereby fulfilling the second condition. As expected, the male''s share of care, and rate of provisioning, were positively related to his share of paternity. The suggestion that the timing of removal was the cue used by males to predict their share of paternity was supported, since after the influence of this variable was controlled, there was no longer any relationship between paternity and paternal care. These data provide qualitative support for optimality models of paternal care in relation to certainty of paternity, and suggest that quantitative tests of the models are possible in well-characterized systems.     

Sperm competition games played by dimorphic male beetles

Reproductive strategies often consist of two alternative tactics whereby males either compete for and guard females, or sneak copulations. By their nature, alternative tactics expose males to differing risks of sperm competition; sneaks will always be subject to sperm competition but guards will be subject to sperm competition with low probability, dependent on the number of sneaks. Recent game-theoretical models predict that males in the sneak role should have the greater gametic expenditure but that the disparity in expenditure should decrease with increasing numbers of sneaks. Male dung beetles in the genus Onthophagus can be separated into two morphs: major males have horns and guard females whereas minor males are hornless and sneak copulations. Here we compare testis size and ejaculate characteristics between these alternative morphs. We find that in O. binodis 30% of males are sneaks, and sneaks have larger testes, ejaculate volumes, and longer sperm than guards. In O. taurus 60% of males are sneaks and there are no differences in gametic traits. Our data thus provide empirical support for game-theoretical models of sperm competition.     

Do Female Red-winged Blackbirds Engage in a Mixed Mating Strategy?

Parentage analyses of broods of nestling red-winged blackbirds (Agelaius phoeniceus) revealed that extra-pair fertilizations (EPFs) accounted for 24% of the offspring. 8% of attempted copulations and 13% of male courtship displays during observations of focal females were by extra-pair males. In addition, mates and non-mates often chased and occasionally made physical contact with females; 34% of those chases in which contact was made were extra-pair chases. Females behaved variably during both within-pair and extra-pair events; females crouched less and resisted more frequently during extra-pair courtship than during within-pair courtship. All extra-pair events, whether natural or induced by male removal, were either resisted or accepted by the female. In 318 focal female-hours of observation during the fertilizable period, no female was ever seen in another male's territory soliciting a copulation. In addition, removal of females' mates resulted in frequent extra-pair courtship and copulation; all of these occurred on the removed male's territory. Some females left their mates' territories on occasion — these forays were nearly always off the study area, no female was ever seen copulating with an extra-pair male while on these forays, and neither the frequency nor the duration of female forays correlated with the frequency of extra-pair fertilizations within broods. There were no associations between extra-pair fertilizations and female age, settlement order, nest order, or clutch size. The number of fledglings produced from a nest was significantly positively associated with the number of sires of the brood. Fewer offspring apparently starved in broods that were multiply sired, yet males did not provide courtship feedings during either within-pair or extra-pair copulations, nor was any paternal care provided to young sired through extra-pair matings. The frequency of infertile eggs was low (< 1%); in those instances of infertile eggs the territory owner sired some young in the same nest or another nest on his territory. Fewer broods were a mixture of within-pair and extra-pair paternity than expected by chance. Clear evidence implicating a mixed strategy on the part of females could not be gathered. Because females behaved variably and because not all costs and benefits to females of extra-pair copulations could be measured, it remains possible that female behavior patterns are either (1) part of a mixed strategy, or (2) part of a strategy minimizing the costs of copulation.     

Sperm competition games between sneaks and guards: a comparative analysis using dimorphic male beetles

Sperm competition is widely recognized as a pervasive force of sexual selection. Theory predicts that across species increased risk of sperm competition should favor an increased expenditure on the ejaculate, a prediction for which there is much evidence. Sperm competition games have also been developed specifically for systems in which males adopt the alternative male mating tactics of sneaking copulations or guarding females. These models have not yet been tested in a comparative context, but predict that: across species male expenditure on the ejaculate should increase with increasing probability of a sneak mating; within species, sneaks should have the greater expenditure on the ejaculate; and the disparity in expenditure between sneaks and guards should be greatest in species with moderate risk of a sneak mating, and decline toward parity in species with low or high risk. Beetles in the genus Onthophagus are often characterized by dimorphic male morphologies that reflect the alternative mating tactics of sneak (minor males) and guard (major males). We conducted a comparative analysis across 16 species of male dimorphic onthophagines, finding that testes size increased across species with increasing frequency of the minor male phenotype. Minor males generally had the greater testes size, but across species the disparity between morphs was independent of the frequency of minor males. We present data on testes allometry from two populations of O. taurus that have undergone genetic divergence in the frequency of minor males. Consistent with the comparative analysis, these data support the notion that the relative frequency of sneaks in the population influences male expenditure on the ejaculate.     

Should advertising parental care be honest?

Species with paternal care show less exaggerated sexual ornamentation than those in which males do not care, although direct benefits from paternal care can vastly exceed the indirect benefits of mate choice. Whether condition-dependent handicaps can signal parenting ability is controversial. The good-parent process predicts the evolution of honest signals of parental investment, whereas the differential-allocation model suggests a trade-off between the attractiveness of a mate and his care-provisioning. I show that both alternatives can arise from optimal allocations to advertisement, parental investment and future reproductive value of the male, and that the male''s marginal fitness gain from multiple matings determines which option should apply. The marginal gain is diminishing if opportunities for polygyny or extra-pair copulations are limited. Advertisement is then expected to be modest and honest, indicating genetic quality and condition-dependent parental investment simultaneously. Increasing marginal gains are likely to be related to cases where genetic quality has a significant influence on offspring fitness. This alternative leads to differential allocation with stronger advertisement, more frequent extra-pair copulations, and diminished male care. Reliability is also reduced if allocation benefits have thresholds, e.g. if there is a minimum body condition required for survival, or if females use a polygyny-threshold strategy of mate choice.     

Insemination efficiency of two alternative male mating tactics in the guppy Poecilia reticulata

In this study we compared the insemination efficiency of two alternative mating tactics (courtship and sneak mating) in the guppy Poecilia reticulata by quantifying the number of sperm delivered during a copulation. During a single copulation, guppies delivered between zero and 92% of the sperm available, as determined by mechanically stripping the males'' sperm reserve at rest. The absolute number of sperm delivered after courtship was three times larger than that delivered through sneak mating; nonetheless, the variance was large with both tactics and the two distributions largely overlapped. The number of sperm available at rest increased with male size. With both tactics, the number of sperm delivered was positively correlated with the sperm available. Contrary to courtship copulations, in sneak copulations there was no correlation between the number of sperm delivered and male size. However, once the data were standardized for sperm reserve, small males delivered a larger proportion of their available sperm during sneak copulation. The rate of sexual acts (sigmoid and thrust rate) before copulation was not correlated with the number of sperm available. After the occurrence of a copulation in both the courtship and sneak copulation groups, the sexual activity of the male decreased in proportion to the amount of sperm he previously inseminated.     

Territoriality and fighting in a colonial thrips, Hoplothrips pedicularius, and sexual dimorphism in Thysanoptera

ABSTRACT.

• 1 Hoplothrips pedicularius (Haliday) (Thysanoptera: Phlaeothripidae), a tubuliferan thrips in which males possess greatly enlarged forelegs, lives in colonies on Stereum fungus.
• 2 Females oviposit onto communal egg masses, and males fight by grasping and stabbing with their forelegs in territorial defence of oviposition areas. Prolonged escalated fights occur between males who are of similar size.
• 3 Larger males usually win fights and become dominant at the oviposition area. Dominant males secure 80% of matings, and mate most frequently during oviposition periods, with an ovipositing female.
• 4 Smaller, subordinate males avoid fights and attempt to 'sneak’copulations. However, they occasionally challenge the dominant male. Challenges tend to follow copulations by the subordinate male and occur more frequently between males who are of similar size.
• 5 Subordinate males who eventually leave the oviposition area are larger than those who remain, have frequently challenged the dominant male, and have more frequently been stabbed.
• 6 Sexual dimorphism in thrips is associated with gregariousness, claustral habitats, female-biased sex ratios, and male winglessness. In thrips genera in which males exhibit foreleg armature, males are larger relative to females. The ecological circumstances promoting sexual dimorphism and male fighting in spatially-structured populations are discussed.

     

Tactic-dependent plasticity in ejaculate traits in the swordtail Xiphophorus nigrensis

In species with alternative reproductive tactics, males that sneak copulations often have larger, higher quality ejaculates relative to males that defend females or nest sites. Ejaculate traits can, however, exhibit substantial phenotypic plasticity depending on a male's mating role in sperm competition, which may depend on the tactic of his competitor. We tested whether exposure to males of different tactics affected sperm number and quality in the swordtail Xipophorus nigrensis, a species with small males that sneak copulations and large males that court females. Sperm swimming speed was higher when the perceived competitor was small than when the competitor was large. Plasticity, however, was only exhibited by small males. Sperm number and viability were invariant between social environments. Our results suggest sperm quality is role-dependent and that plastic responses to the social environment can differ between male reproductive tactics.     

Experience Matters: Females Use Smell to Select Experienced Males for Paternal Care

Mate choice and mating preferences often rely on the information content of signals exchanged between potential partners. In species where a female''s reproduction is the terminal event in life it is to be expected that females choose high quality males and assess males using some honest indicator of male quality. The Nereidid polychaete, Neanthes acuminata, exhibits monogamous pairing and the release of eggs by females terminates her life and larval success relies entirely on a male''s ability to provide paternal care. As such females should have developed reliable, condition-dependent criteria to choose mates to guarantee survival and care for offspring. We show that females actively chose males experienced in fatherhood over others. In the absence of experienced males dominance, as evident from male-male fights, is utilized for mate selection. The preference for experienced males is not affected by previous social interactions between the individuals. We show that the choice of the partner is based on chemical signals demonstrating a ‘scent of experience’ to females providing evidence for the role of chemical signals in sexual selection for paternal care adding to our understanding of the mechanisms regulating condition-dependent mate choice.     

Strategic paternity assurance in the sex-role reversed Eurasian dotterel (Charadrius morinellus): behavioral and genetic evidence

Sex role reversal in birds is usually associated with paternalcare of both eggs and chicks. This pattern of care typicallyleads to the potential rate of reproduction of males being lowerthan that of females. Hence, operational sex-ratio theory predictsthat each male should be under strong selection to avoid beingcuckolded. A male should, therefore, guard his female partner(s)from extrapair copulation attempts by other males. Furthermore,the sexual conflict theory of copulation behavior predicts thatin species with extensive paternal care the male should controlthe temporal pattern of copulations—copulations shouldoccur both frequently and throughout the prelaying period. Wetested these predictions in the Eurasian dotterel (Charadriusmorinsllus), in which the male usually provides all the parentalcare. In accordance with the first prediction, male dotterelsdid "guard" their pair-female prior to egg-laying. Contraryto the second prediction, however, copulations were not frequentand did not occur throughout the pre-laying phase-despite frequentsolicitation by the female, copulations only occurred immediatelyprior to egg-laying. Nevertheless, male-initiated courtshipwas both coincident with the pattern of copulations and morelikely than female-initiated courtship to result in copulation.Our results do, therefore, appear to agree with the centralprediction of the sexual conflict theory that males should controlthe pattern of copulations. We suggest that male dotterels willcopulate only after several days of being paired because theyface a duel risk of cuckoldry from both extrapair copulationand rapid mate switching. We tested the realized incidence ofcuckoldry using DNA fingerprinting. Only 4.6% (2/44) of chickswere not the genetic offspring of the caring male correspondingto 9.1% (2/22) broods affected. The rate of extrapair paternityin the dotterel is, therefore, relatively low compared to thatin many other avian species. We conclude that male dotterelssuccessfully protect their paternity of the brood for whichthey care through a combined strategy of mate guarding and strategictiming of copulations.     

Parasitic spawning in sand gobies: an experimental assessment of nest-opening size, sneaker male cues, paternity, and filial cannibalism

Sneaking is common in nest-building fish with paternal care,but the role of nest-opening size in protecting against entryby sneaker males has never been tested before. Using the sandgoby (Pomatoschistus minutus), a fish with exclusive paternalcare, experimental manipulations of nest openings provided nosupport for the hypothesis that nest openings serve as physicalor visual defense or that sneaker males prefer to parasitizenests with wide openings. Female mating preference was alsonot influenced by nest-opening size. However, female courtshipbehavior and visibility were important cues for sneaker males.Most sneak entries occurred when the nest holder was occupiedwith courtship, chasing another sneaker male or nest building.In half the cases of observed sneak entry, the sneaker malefertilized eggs, also when sneaking only occurred before spawning.Sneak entry and its duration were good estimates of stolen paternity,but neither sneak entries nor degree of fertilizations werecorrelated with filial cannibalistic behavior. Testes size didnot explain parasitic spawning success in replicates with geneticallydetermined sneaking. However, all sneaker males without breedingcoloration had huge testes and small sperm duct glands, whereasnest-holding males had small testes and large sperm duct glands,and sneaker males with breeding coloration were intermediate.     

Paternity uncertainty overrides sex chromosome selection for preferential grandparenting

With respect to autosomal genes, a grandparent is equally related to male and female grandchildren. Because males are heterozygous for sex chromosomes, however, grandparents are asymmetrically related to male and female grandchildren via the sex chromosomes. For example, the Y chromosome from the paternal grandfather passes directly down to grandsons. This asymmetry leads to a prediction that genes on the sex chromosomes could drive differential grandparental care. Alternatively, the paternity uncertainty hypothesis for differential grandparent care brings about a different set of predictions. A grandfather, for example, has two degrees of uncertainty to his son's children but only one to his daughter's children. Thus, under high extra-pair paternity rates, paternity uncertainty predicts that a grandfather will favor his daughter's children over his son's children. A paternity uncertainty vs. a genetic relatedness hypothesis was tested using data from questionnaires asking adult grandchildren to rate the amount and quality of care of their various grandparents. We found no support for preferential care based on expected sex chromosome similarities. Instead, our data were in general accord with the predictions of the paternity uncertainty hypothesis of grandparental care. A model is presented to predict the rates of extra-pair paternity required in a population to have the effects of paternity uncertainty outweigh sex chromosome effects.     

Faithful females receive more help: the extent of male parental care during incubation in relation to extra‐pair paternity in songbirds

Parental care provided by males occurs in a diverse array of animals and there are large differences among species in its extent compared with female care. However, social and ecological factors responsible for interspecific differences in male's share of parental duties remain unclear. Genetic fidelity of females has been long considered important. Theory predicts that females should receive more help from their mates in raising the offspring in species with high genetic fidelity. Using avian incubation behaviour as a model system, we confirmed this prediction. The extent of male's help during incubation increased with decreasing rate of extra‐pair paternity across species (22 species of socially monogamous songbirds from 13 families; male's share of incubation ranged from 6% to 58%), even after accounting for covariates, biases in species selection and intraspecific variability. Moreover, this result was not sensitive to two different phylogenies and branch length estimates. We suggest that our findings support the notion, backed by theory, that genetic fidelity is an important factor in the evolution of male parental care. We offer several behavioural scenarios for the coevolution between male's share of parental duties and the genetic mating system.     

Quantitative genetic evidence that males trade attractiveness for ejaculate quality in guppies

Polyandry, where females mate with multiple males, means that a male''s reproductive success will depend both on his ability to acquire mates and the ability of his sperm to compete effectively for fertilizations. But, how do males partition their reproductive investment between these two episodes of selection? Theory predicts that increases in ejaculate investment will come at a cost to investment in other reproductive traits. Although evidence revealing such trade-offs is accumulating, we know little about their genetic basis. Here, I report patterns of genetic (co)variation for a range of traits subject to pre- and post-copulatory sexual selection in the guppy Poecilia reticulata, a promiscuous livebearing fish in which males alternate between courtship and sneak matings to obtain copulations. The analyses of genetic variation and covariation for these behaviours revealed a strong genetic predisposition for one tactic over the other. Both mating tactics were also strongly genetically integrated with the level of sexual ornamentation and ejaculate quality. Males that predominantly performed sneak matings were less ornamented but had faster swimming sperm than those that predominantly used courtship. These patterns of genetic variation and covariation reveal potential evolutionary constraints on the direction of selection of pre- and post-copulatory traits, and support sperm competition theory by revealing a trade-off between sexual attractiveness and investment in ejaculates.     

High rates of extra‐pair paternity in a socially monogamous beetle with biparental care

1. Nest construction and paternity assurance are predicted to favour biparental care in insects. The horned passalus (Odontotaenius disjunctus) is a socially monogamous beetle with biparental care that breeds in decaying logs. The genetic mating system of the horned passalus was investigated to determine if paternity assurance is likely to drive the evolution or maintenance of paternal care in this system. Parental time budgets were also examined to better understand the types and frequencies of behaviours performed by parents. 2. Genotyping‐by‐sequencing revealed high levels of extra‐pair paternity, with 54.8% of offspring sired by extra‐pair males and 70% of nests containing extra‐pair young. 3. More heterozygous social males were cuckolded less than more homozygous social males. Extra‐pair mating, however, seems unlikely to increase offspring genetic diversity as extra‐pair offspring were not more heterozygous than within‐pair offspring, and average brood heterozygosity did not increase with higher rates of extra‐pair paternity. 4. Behavioural observations demonstrated that parents spent on average 46.5% of their time processing the decaying wood resource for larval offspring. Because resource processing is a by‐product of feeding and provides shareable benefits for all larvae in the brood, this form of paternal care could be favoured despite low paternity.     

Male reed buntings do not adjust parental effort in relation to extrapair paternity

Parental effort is considered to be costly; therefore, malesare expected to provide less care to unrelated offspring. Theoreticalmodels suggest that males should either reduce their care tothe entire brood or alternatively distinguish between relatedand unrelated nestlings and direct provisioning to kin whenpaternity is in doubt. Reed buntings (Emberiza schoeniclus)have been found to have high levels of extrapair paternity (EPP,i.e., offspring of a male other than the male attending thenest; 55% of offspring), and males are therefore under strongselection pressure to adjust their parental effort accordingto the proportion of EPP in their brood. In this study, we investigatedwhether male reed buntings exhibit a reduction in paternal care(incubation and provisioning nestlings) in relation to decreasedpaternity. We also assess whether males bias their provisioningtoward kin. We measured incubation time, provisioning rates,and food allocation to individual nestlings using video recordingsat the nests. Microsatellite DNA analysis was used to analyzethe paternity of offspring. In direct contrast to a previousstudy on the same species, our results provided no indicationthat males lowered their effort with decreased paternity. Furthermore,in nests of mixed paternity, males did not bias their provisioningbehavior to kin. It remains to be investigated whether the absenceof a relationship between paternity and paternal care can beascribed to absence of reliable paternity cues or whether thebenefits of reducing paternal care did not outweigh the costsin our study population. We found no evidence that the levelof paternal care affected male survival or offspring mass, suggestingthat both the benefits and costs of any reduction in paternalcare would have been low.     

Male sperm expenditure under sperm competition risk and intensity in quacking frogs

In the frog Crinia georgiana, reproductive behavior comprisesa "guarding tactic," in which males defend spawn sites and attractfemales by calling, and a "sneak tactic," in which males joinspawning pairs. The aims of the present study were to (1) relateejaculate expenditure by "guarding" and "sneak" males to theirprobability of mating with other males present (sperm-competitionrisk), and (2) determine if males adjust their ejaculate expenditureaccording to the number of males involved in a spawning (sperm-competitionintensity). Theory predicts that because sneak males alwaysmate with other males present, they will experience a highersperm-competition risk and should release larger ejaculatesrelative to that of guarding males. However, as the proportionof sneaks in a population increases so does the risk of spermcompetition to guarders, so expenditure by each tactic shouldmove toward equality. Given that the incidence of sneak behavioris high in C. georgiana, guarders and sneaks were expected toexperience similar risks of sperm competition and show similarinvestment in spermatogenesis. Comparison of testes size andejaculate size showed no difference between tactics. Modelsof sperm-competition intensity predict that males should increasetheir ejaculate size when spawning in the presence of one othermale but decrease their ejaculate size when spawning in thepresence of multiple males. Here, males maintained a constantsperm number irrespective of whether a mating involved one,two, or three males. This result suggests that male C. georgianado not facultatively adjust ejaculate investment in responseto fluctuating intensities of sperm competition.     

Last–male sperm precedence in the bushcricket Poecilimon veluchianus (Orthoptera, Tettigonioidea) demonstrated by DNA fingerprinting

Males of the bushcricket Poecilimon veluchianus pass a large spermatophore to the female during mating. The spermatophore is eaten by the female after copulation. Because females mate with several males during their reproductive life, the competition between spermatozoa of different males affects a male's reproductive success. In order to determine the outcome of sperm competition, the paternity of the progeny of double–mated females was established by DNA fingerprinting with the oligonucleotide (GATA)₄. Typical P. veluchianus DNA fingerprints consisted of 15 scoreable fragments per individual. The proportion of bands shared between presumably unrelated bushcrickets was 17%. After the second copulation the second mating male clearly predominated at fertilization. The mean proportion of eggs fertilized by the second male was 90.1%. There was no significant relationship between the level of sperm precedence and the time of ovipositions after the second mating. If female P. veluchianus increase the fitness of their offspring by the incorporation of spermatophore–derived substances in developing eggs, there is little chance for the feeding male to fertilize eggs containing his nutrients, because of the very short mating intervals of females and the observed high level of last–male sperm precedence in this species. Under such conditions the last mating male would fertilize many eggs containing nutrients from a prior male. Because nuptial gifts, like the tettigoniid spermatophore, function only as paternal investment if the donating male's progeny benefit from the gift, a paternal investment function of the P. veluchianus spermatophore seems to be unlikely.     

The unexpected but understandable dynamics of mating,paternity and paternal care in the ocellated wrasse

Although theory generally predicts that males should reduce paternal care in response to cues that predict increased sperm competition and decreased paternity, empirical patterns are equivocal. Some studies have found the predicted decrease in male care with increased sperm competition, while even more studies report no effect of paternity or sperm competition on male care. Here, we report the first example, to our knowledge, of paternal care increasing with the risk and intensity of sperm competition, in the ocellated wrasse (Symphodus ocellatus). Theory also predicts that if paternal care varies and is important to female fitness, female choice among males and male indicators traits of expected paternal care should evolve. Despite a non-random distribution of mating success among nests, we found no evidence for female choice among parental males. Finally, we document the highest published levels of extra-pair paternity for a species with exclusive and obligate male care: genetic paternity analyses revealed cuckoldry at 100 per cent of nests and 28 per cent of all offspring were not sired by the male caring for them. While not predicted by any existing theory, these unexpected reproductive patterns become understandable if we consider how male and female mating and parental care interact simultaneously in this and probably many other species.     

Explicit experimental evidence for the role of mate guarding in minimizing loss of paternity in the Seychelles warbler

Extra-pair copulations (EPCs) (copulations outside the pair bond) resulting in extra-pair fertilizations (EPFs) are widespread in birds. To increase reproductive success, males should not only seek EPCs, but also prevent their females from having EPFs. Male Seychelles warblers (Acrocephalus sechellensis) follow their partner closely during the period when these females are most receptive (fertile period). The Seychelles warbler is the first species to offer explicit experimental evidence that mate guarding functions as paternity guarding: in territories where free-living males were induced to stop mate guarding during the pair female''s fertile period, the rates of intrusions by other males and successful EPCs (male mounting female) were significantly higher than those observed in the control group and in the absence of mate guarding the frequency of successful EPCs increased significantly with local male density. Male warblers do not assure their paternity through frequent copulations to devalue any sperm from other males: males do not copulate with their partners immediately following a successful EPC obtained by their partners, the frequency of successful within-pair copulations does not increase with the frequency of successful EPCs and females initiate all successful copulations and are capable of resisting copulation attempts.