Siring Success Research Articles

Post-copulatory sexual selection allows females to alleviate the fitness costs incurred when mating with senescing males.

Male senescence has detrimental effects on reproductive success and offspring fitness. When females mate with multiple males during the same reproductive bout, post-copulatory sexual selection that operates either through sperm competition or cryptic female choice might allow females to skew fertilization success towards young males and as such limit the fitness costs incurred when eggs are fertilized by senescing males. Here, we experimentally tested this hypothesis. We artificially inseminated female North African houbara bustards with sperm from dyads of males of different (young and old) or similar ages (either young or old). Then, we assessed whether siring success was biased towards young males and we measured several life-history traits of the progeny to evaluate the fitness costs due to advanced paternal age. In agreement with the prediction, we found that siring success was biased towards young males, and offspring sired by old males had impaired hatching success, growth and post-release survival (in females). Overall, our results support the hypothesis that post-copulatory sexual selection might represent an effective mechanism allowing females to avoid the fitness costs of fertilization by senescing partners.

Density-dependent decline of early horn growth in European mouflon

The development of horns in Caprinae can be largely influenced by food-limiting factors such as population density and climate, as well as by negative evolutionary responses to size-selective harvesting. In this study, we investigated the effects of population density, environmental covariates and trophy hunting on horn development in a population of European mouflon Ovis aries musimon introduced to the Mediterranean region of Croatia in the early 1980s. The study population was subject to commercial trophy hunting on males since the mid-1980s. This allowed to analyse the temporal trend in early horn growth in 341 rams legally culled. Cohort-based linear model and analysis of deviance (ANODEV) revealed a significant negative trend in early horn growth, with a decline of ca. 10% over only 15 cohorts (1993–2007). The increase in population density (by ca. 600%) and summer temperature, selected via LASSO regression, explained about 61% and 13% of the decline in early horn growth, as revealed by the ANODEV R2. Our results suggest a prominent role of food-limiting factors in the decline of weapon size. We also found a negative relationship between age at death and early horn growth in our study population, which suggests the occurrence of hunters’ selectivity towards large horns. The effect of trophy hunting on the decline in horn size, however, is difficult to quantify. Our analysis was largely influenced by the rapid increase of mouflon density after introduction, thereby limiting the possibility to detect potential effects of hunting selection, although the large number of rams shot before 5 years of age may possibly lead to undesirable consequences of trophy hunting on mating success. To clarify the consequences of commercial trophy hunting on the mouflon population, the long-term pattern of horn growth and the age-dependent male siring success should be further investigated.

Long-term studies of bighorn sheep and mountain goats reveal fitness costs of reproduction.

Fitness costs of reproduction are expected when resources are limited. Costs drive the evolution of life-history strategies and can affect population dynamics if females change their allocation of resources to reproduction. We studied fitness costs of reproduction in mountain ungulates in Alberta, Canada. We monitored two populations of bighorn sheep (Ovis canadensis) for 44 and 30years, and one of mountain goats (Oreamnos americanus) for 30years. Both species are highly iteroparous. Heterogeneity in individual reproductive potential makes fitness costs of reproduction difficult to detect and quantify without manipulations. In capital breeders, individual differences can be partly accounted for by considering body mass and other correlates of reproductive potential. Long-term monitoring can reveal costs that only manifest under stressful conditions such as disease or resource scarcity. Despite individual differences in reproductive potential, we detected fitness costs of reproduction in females. Costs, in terms of mass gain and survival, are almost entirely born by subsequent offspring, as mothers prioritize their own maintenance and survival. Costs are greater for primiparous females, decrease with increasing body mass and increase as resource availability declines, and sons are costlier than daughters. Costs may increase for senescent females that appear to reduce allocation to reproduction. In bighorn sheep, costs mostly involve reduced mass gain and lower survival of subsequent offspring. In mountain goats, costs include reductions in mass gain, subsequent fecundity and juvenile survival. In males, fitness costs derive mostly from attempts to reproduce rather than from siring success and likely depend upon individual competitiveness. In the absence of selective harvests, dominant males may enjoy high fitness and possibly lower costs compared to subordinates. The conservative reproductive tactic of mountain ungulate females likely explains why density dependence mostly involves later primiparity and lower recruitment, but rarely affects adult survival. Future research will seek to better account for heterogeneity in reproductive potential, assess cumulative reproductive costs and investigate the potential effects of fathers on maternal allocation tactics.

Male-only care and cuckoldry in black coucals: does parenting hamper sex life?

Providing parental care often reduces additional mating opportunities. Paternal care becomes easier to understand if trade-offs between mating and caring remain mild. The black coucal Centropus grillii combines male-only parental care with 50% of all broods containing young sired by another male. To understand how much caring for offspring reduces a male's chance to sire additional young in other males' nests, we matched the production of extra-pair young in each nest with the periods during which potential extra-pair sires were either caring for offspring themselves or when they had no own offspring to care for. We found that males which cared for a clutch were not fully excluded from the pool of competitors for siring young in other males' nests. Instead, the relative siring success showed a temporary dip. Males were approximately 17% less likely to sire young in other males' nests while they were incubating, about 48% less likely to do so while feeding nestlings, followed by 26% when feeding fledglings, compared to the success of males that currently did not care for offspring. These results suggest that real-life care situations by males may involve trade-off structures that differ from, and are less strict than those frequently employed in theoretical considerations of operational sex ratios, sex roles and parenting decisions.

Rapid loss of self-incompatibility in experimental populations of the perennial outcrossing plant Linaria cavanillesii.

Transitions from self-incompatibility to self-compatibility in angiosperms may be frequently driven by selection for reproductive assurance when mates or pollinators are rare, and are often succeeded by loss of inbreeding depression by purging. Here, we use experimental evolution to investigate the spread of self-compatibility from one such population of the perennial plant Linaria cavanillesii into self-incompatible (SI) populations that still have high inbreeding depression. We introduced self-compatible (SC) individuals at different frequencies into replicate experimental populations of L. cavanillesii that varied in access to pollinators. Our experiment revealed a rapid shift to self-compatibility in all replicates, driven by both greater seed set and greater outcross siring success of SC individuals. We discuss our results in the light of computer simulations that confirm the tendency of self-compatibility to spread into SI populations under the observed conditions. Our study illustrates the ease with which self-compatibility can spread among populations, a requisite for species-wide transitions from self-incompatibility to self-compatibility.

No evidence for prezygotic postcopulatory avoidance of kin despite high inbreeding depression.

Offspring resulting from mating among close relatives can suffer from impaired fitness through the expression of recessive alleles with deleterious effects. Postcopulatory sperm selection (a prezygotic mechanism of cryptic female choice) has been suggested to be an effective way to avoid inbreeding. To investigate whether postcopulatory female choice allows the avoidance of fertilization by close kin, we performed artificial inseminations in a promiscuous bird, the houbara bustard (Chlamydotis undulata undulata). Females were inseminated with a mix of sperm from triads of males, each constituted of a male genetically unrelated to the female, a first cousin and a half-sibling. When counting the number of eggs sired by unrelated males, cousins or half-siblings, we found a significant deviation from the expected random distribution, with more eggs sired by unrelated males. However, offspring sired by cousins, and especially by half-siblings suffered from high prehatching mortality, suggesting that the observed paternity skew towards unrelated males might reflect differential offspring mortality rather than sperm selection. In agreement with this hypothesis, within-triad siring success was similar for the three parental relatedness categories, but the relationship between siring and hatching success differed across categories. In clutches with high hatching success, unrelated males had the highest success while in clutches with high failure rate, half-siblings had the highest success. Offspring sired by half-siblings also suffered from reduced growth rate during the first three months and higher posthatching mortality. Hence, despite substantial fitness costs associated with fertilization by close relatives, females do not seem to select sperm of unrelated males.

Mating pattern of a distylous primrose in a natural population: unilateral outcrossing and asymmetric selfing between sexual morphs

Heterostyly is a genetic polymorphism of anther and stigma heights, which are reciprocally placed among morphs. The maintenance of heterostyly has often been ascribed to disassortative mating, but alternative explanations are also possible, which can be examined by analyzing mating patterns. However, parental analysis with genetic markers has only been applied to a limited number of taxa, despite the phylogenetic diversity of heterostylous species. Here, we examined the mating patterns of a distylous primrose, Primula kisoana (Primulaceae), in its natural habitat, using 11 microsatellite markers. We also examined other fitness components. We found no differences in seed production, vegetative growth, or survival between morphs. However, the siring success of thrum fathers was much higher than that of pin fathers; outcrossing occurred unilaterally between thrum fathers and pin mothers, and selfing was more frequent in thrum plants than in pin plants. These findings are consistent with the explanation that distyly in this species is maintained either by overdominance due to previously reported recessive lethal effects of the thrum allele or by effectively dioecious mating if inbreeding depression is strong. We built a mathematical model of the overdominance hypothesis to confirm that it is logically sound. These results warrant further investigations into the possible roles of overdominance and dioecy in the maintenance of heterostyly.

Mating consequences of contrasting hermaphroditic plant sexual systems.

For hermaphroditic angiosperms with multiple flowers, the sex roles can be exclusively combined in bisexual flowers (monocliny), strictly separated among different flowers (monoecy), or arrayed in mixtures of bisexual flowers with female flowers (gynomonoecy) or male flowers (andromonoecy). The hypothesized benefits favoring the evolution of these contrasting hermaphroditic sexual systems are typically examined individually, usually by assessing success through only one sex role. We tested predictions of most hypotheses experimentally with an andromonoecious species, Anticlea occidentalis (Melanthiaceae), based on the performance of intact plants (andromonoecy) and those with emasculated bisexual flowers (functionally monoecious) or emasculated male flowers (functionally monoclinous with sterile peripheral flowers). Andromonoecy in this species enables efficient, size-dependent resource allocation, emphasizing female function in large plants. Emasculation revealed that anthers in male flowers promote female mating quality (outcrossing rate and mate diversity), whereas anthers in bisexual flowers promote male mating quantity (pollen dispersal distance and probability of any siring success). Thus, different hermaphroditic sexual systems likely evolve to capitalize on suites of benefits, rather than just one, and provide compromises between quantitative and qualitative reproductive components. These compromises apparently maximize an individual's combined genetic contributions through female and male functions, rather than separate contributions through each sex role.

Optimal sperm length for high siring success depends on forehead patch size in collared flycatchers

Dominance over rivals, sexual attractiveness, and highly efficient ejaculates are 3 important contributors of male fertilization success but theories about how primary and secondary sexual characte ...

Male Body Size Predicts Reproductive Success But Not Within-Clutch Paternity Patterns in Gopher Tortoises (Gopherus polyphemus).

In many vertebrates, body size is an important driver of variation in male reproductive success. Larger, more fit individuals are more likely to dominate mating opportunities, skewing siring success and resulting in lower effective population sizes and genetic diversity. The mating system of the gopher tortoise (Gopherus polyphemus) has been characterized as both female-defense and scramble-competition polygyny. Mating systems are typically not fixed and can be influenced by factors such as population density, demographic structure, and environmental conditions; however, most populations will have a predominant strategy that results from local conditions. We assessed how male body size influences patterns of paternity and reproductive success in a natural population of gopher tortoises in Florida, United States. Using microsatellites, we assigned parentage of 220 hatchlings from 31 nests collected during 2 reproductive seasons. Larger males were significantly more likely to sire offspring and sired more offspring than smaller males; however, the likelihood of a clutch being multiply sired was unrelated to male body size. We also found evidence of mate fidelity across years. Although paternity patterns in this high-density population are more consistent with defense polygyny, female monopoly by males was incomplete, with both large and small males contributing to multiply sired clutches. Additional behavioral data are needed to clarify the role of female mate selection in paternity outcomes. The context-dependence of mating systems underscores the need to compare parentage patterns across populations and to recognize the potential for more than 1 strategy to be employed within a single population.

On the ecological significance of pollen color: a case study in American trout lily (Erythronium americanum).

Evolutionary ecologists seek to explain the processes that maintain variation within populations. In plants, petal color variation can affect pollinator visitation, environmental tolerance, and herbivore deterrence. Variation in sexual organs may similarly affect plant performance. Within-population variation in pollen color, as occurs in the eastern North American spring ephemeral Erythronium americanum, provides an excellent opportunity to investigate the maintenance of variation in this trait. Although the red/yellow pollen-color polymorphism of E.americanum is widely recognized, it has been poorly documented. Our goals were thus (1) to determine the geographic distribution of the color morphs and (2) to test the effects of pollen color on components of pollen performance. Data provided by citizen scientists indicated that populations range from monomorphic red, to polymorphic, to monomorphic yellow, but there was no detectable geographic pattern in morph distribution, suggesting morph occurrence cannot be explained by a broad-scale ecological cline. In field experiments, we found no effect of pollen color on the probability of predation by the pollen-feeding beetle Asclera ruficollis, on the ability of pollen to tolerate UV-B radiation, or on siring success (as measured by the fruit set of hand-pollinated flowers). Pollinators, however, exhibited site-specific pollen-color preferences, suggesting they may act as agents of selection on this trait, and, depending on the constancy of their preferences, could contribute to the maintenance of variation. Collectively, our results eliminate some hypothesized ecological effects of pollen color in E.americanum, and identify effects of pollen color on pollinator attraction as a promising direction for future investigation.

Pollen competition between morphs in a pollen-color dimorphic herb and the loss of phenotypic polymorphism within populations.

Flower color polymorphism is relatively uncommon in natural flowering plants, suggesting that maintenance of different color morphs within populations is difficult. To address the selective mechanisms shaping pollen-color dimorphism, pollinator preferences and reproductive performance were studied over three years in Epimedium pubescens in which some populations had plants with either green or yellow pollen (and anthers). Visitation rate and pollen removal and receipt by the bee pollinator (Andrena emeishanica) did not differ between the two color morphs. Compared to the green morph, siring success of the yellow morph's pollen was lower, but that of mixtures of pollen from green and yellow morphs was lowest. This difference, corresponding to in vivo and ex vivo experiments on pollen performance, indicated that pollen germination, rather than tube growth, of the green morph was higher than that of the yellow morph and was seriously constrained in both morphs if a pollen competitor was present. A rare green morph may invade a yellow-morph population, but the coexistence of pollen color variants is complicated by the reduced siring success of mixed pollinations. Potential pollen competition between morphs may have discouraged the maintenance of multiple phenotypes within populations, a cryptic mechanism of competitive exclusion.

Divergence in pollen performance between Clarkia sister species with contrasting mating systems supports predictions of sexual selection.

Animal taxa that differ in the intensity of sperm competition often differ in sperm production or swimming speed, arguably due to sexual selection on postcopulatory male traits affecting siring success. In plants, closely related self- and cross-pollinated taxa similarly differ in the opportunity for sexual selection among male gametophytes after pollination, so traits such as the proportion of pollen on the stigma that rapidly enters the style and mean pollen tube growth rate (PTGR) are predicted to diverge between them. To date, no studies have tested this prediction in multiple plant populations under uniform conditions. We tested for differences in pollen performance in greenhouse-raised populations of two Clarkia sister species: the predominantly outcrossing C. unguiculata and the facultatively self-pollinating C. exilis. Within populations of each taxon, groups of individuals were reciprocally pollinated (n = 1153 pollinations) and their styles examined four hours later. We tested for the effects of species, population, pollen type (self vs. outcross), the number of competing pollen grains, and temperature on pollen performance. Clarkia unguiculata exhibited higher mean PTGR than C. exilis; pollen type had no effect on performance in either taxon. The difference between these species in PTGR is consistent with predictions of sexual selection theory.

Phenological match drives pollen-mediated gene flow in a temporally dimorphic tree.

Variation in flowering phenology is common in natural populations, and is expected to be, together with inter-mate distance, an important driver of effective pollen dispersal. In populations composed of plants with temporally separated sexual phases (i.e. dichogamous or heterodichogamous populations), pollen-mediated gene flow is assumed to reflect phenological overlap between complementary sexual phases. In this study, we conducted paternity analyses to test this hypothesis in the temporally dimorphic tree Acer opalus. We performed spatially explicit analyses based on categorical and fractional paternity assignment, and included tree size, pair-wise genetic relatedness and morph type as additional predictors. Because differences between morphs in flowering phenology may also influence pollination distances, we modelled separate pollen dispersal kernels for the two morphs. Extended phenological overlap between male and female phases (mainly associated with inter-morph crosses) resulted in higher siring success after accounting for the effects of genetic relatedness, morph type and tree size, while reduced phenological overlap (mainly associated with intra-morph crosses) resulted in longer pollination distances achieved. Siring success also increased in larger trees. Mating patterns could not be predicted by phenology alone. However, as heterogeneity in flowering phenology was the single morph-specific predictor of siring success, it is expected to be key in maintaining the temporal dimorphism in A.opalus, by promoting not only a prevalent pattern of inter-morph mating, but also long-distance pollination resulting from intra-morph mating events.

Sexually antagonistic evolution caused by male-male competition in the pistil.

Although sexual selection and sexual conflict are important evolutionary forces in animals, their significance in plants is uncertain. In hermaphroditic organisms, such as many plants, sexual conflict may occur both between mating partners (interlocus conflict) and between male and female sex roles within an individual (intralocus conflict). We performed experimental evolution, involving lines that were crossed with either one or two pollen donors (monogamous or polyandrous lines), in the hermaphroditic plant (Collinsia heterophylla) where early fertilizations are associated with female fitness costs (reduced seed set). Artificial polyandry for four generations resulted in enhanced pollen performance and increased female fitness costs compared to the monogamous and source (starting material) lines. Female fitness was also reduced in the monogamous line, indicating a possible trade-off between sex roles, resulting from early pollination. We performed a second experiment to investigate a potential harming effect of pollen performance on seed set. We found that high siring success of early arriving pollen competing with later-arriving pollen was associated with high female fitness costs, consistent with an interlocus sexual conflict. Our study provides evidence for the importance of sexual selection in shaping evolution of plant reproductive strategies, but also pinpoints the complexity of sexual conflict in hermaphroditic species.

A sex-chromosome inversion causes strong overdominance for sperm traits that affect siring success.

Male reproductive success depends on the competitive ability of sperm to fertilize the ova, which should lead to strong selection on sperm characteristics. This raises the question of how heritable variation in sperm traits is maintained. Here we show that in zebra finches (Taeniopygia guttata) nearly half of the variance in sperm morphology is explained by an inversion on the Z chromosome with a 40% allele frequency in the wild. The sperm of males that are heterozygous for the inversion had the longest midpieces and the highest velocity. Furthermore, such males achieved the highest fertility and the highest siring success, both within-pair and extra-pair. Males homozygous for the derived allele show detrimental sperm characteristics and the lowest siring success. Our results suggest heterozygote advantage as the mechanism that maintains the inversion polymorphism and hence variance in sperm design and in fitness.

Age-dependent trajectories differ between within-pair and extra-pair paternity success.

Reproductive success is associated with age in many taxa, increasing in early life followed by reproductive senescence. In socially monogamous but genetically polygamous species, this generates the interesting possibility of differential trajectories of within-pair and extra-pair siring success with age in males. We investigate these relationships simultaneously using within-individual analyses with 13years of data from an insular house sparrow (Passer domesticus) population. As expected, we found that both within- and extra-pair paternity success increased with age, followed by a senescence-like decline. However, the age trajectories of within- and extra-pair paternity successes differed significantly, with the extra-pair paternity success increasing faster, although not significantly, in early life, and showing a delayed decline by 1.5years on average later in life compared to within-pair paternity success. These different trajectories indicate that the two alternative mating tactics should have age-dependent pay-offs. Males may partition their reproductive effort between within- and extra-pair matings depending on their current age to reap the maximal combined benefit from both strategies. The interplay between these mating strategies and age-specific mortality may explain the variation in rates of extra-pair paternity observed within and between species.

Mating System Evolution under Strong Pollen Limitation: Evidence of Disruptive Selection through Male and Female Fitness in Clarkia xantiana.

Selection on floral traits in hermaphroditic plants is determined by both male and female reproductive success. However, predictions regarding floral trait and mating system evolution are often based solely on female fitness. Selection via male fitness has the potential to affect the outcomes of floral evolution. In this study, we used paternity analysis to assess individual selfing rates and selection on floral traits via male and female fitness in an experimental population of Clarkia xantiana where pollen limitation of seed set was strong. We detected selection through both female and male fitness with reinforcing or noninterfering patterns of selection through the two sex functions. For female fitness, selection favored reduced herkogamy and protandry, traits that promote increased autonomous selfing. For male fitness, selection on petal area was disruptive, with higher trait values conferring greater pollinator attraction and outcross siring success and smaller trait values leading to higher selfed siring success. Combining both female and male fitness, selection on petal area and protandry was disruptive because intermediate phenotypes were less successful as both males and females. Finally, functional relationships among male and female fertility components indicated that selfing resulted in seed discounting and pollen discounting. Under these functional relationships, the evolutionarily stable selfing rate can be intermediate or predominantly selfing or outcrossing, depending on the segregating load of deleterious mutations.

Ovule positions within linear fruit are correlated with nonrandom mating in Robinia pseudoacacia.

Post-pollination processes can lead to nonrandom mating among compatible pollen donors. Moreover, morphological patterns of ovule development within linear fruits are reportedly nonrandom and depend on ovule position. However, little is known about the relationship between nonrandom mating and ovule position within linear fruit. Here, we combined controlled pollen competition experiments and paternity analyses on R. pseudoacacia to better understand nonrandom mating and its connection with ovule position. Molecular determination of siring success showed a significant departure from the expected ratio based on each kind of pollen mixture, suggesting a nonrandom mating. Outcrossed pollen grains, which were strongly favored, produced significantly more progeny than other pollen grains. Paternity analyses further revealed that the distribution of offspring produced by one specific pollen source was also nonrandom within linear fruit. The stylar end, which has a higher probability of maturation, produced a significantly higher number of outcrossed offspring than other offspring, suggesting a correlation between pollen source and ovule position. Our results suggested that a superior ovule position exists within the linear fruit in R. pseudoacacia, and the pollen that was strongly favored often preferentially occupies the ovules that were situated in a superior position, which ensured siring success and facilitated nonrandom mating.

Sources of (co)variation in alternative siring routes available to male great tits (Parus major).

Males of socially monogamous species can increase their siring success via within-pair and extra-pair fertilizations. In this study, we focused on the different sources of (co)variation between these siring routes, and asked how each contributes to total siring success. We quantified the fertilization routes to siring success, as well as behaviors that have been hypothesized to affect siring success, over a five-year period for a wild population of great tits Parus major. We considered siring success and its fertilization routes as "interactive phenotypes" arising from phenotypic contributions of both members of the social pair. We show that siring success is strongly affected by the fecundity of the social (female) partner. We also demonstrate that a strong positive correlation between extra-pair fertilization success and paternity loss likely constrains the evolution of these two routes. Moreover, we show that more explorative and aggressive males had less extra-pair fertilizations, whereas more explorative females laid larger clutches. This study thus demonstrates that (co)variation in siring routes is caused by multiple factors not necessarily related to characteristics of males. We thereby highlight the importance of acknowledging the multilevel structure of male fertilization routes when studying the evolution of male mating strategies.