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The evolution of polyandry: multiple mating and female fitness in insects.

Theory suggests that male fitness generally increases steadily with mating rate, while one or a few matings are sufficient for females to maximize their reproductive success. Contrary to these predictions, however, females of the majority of insects mate multiply. We performed a meta-analysis of 122 experimental studies addressing the direct effects of multiple mating on female fitness in insects. Our results clearly show that females gain directly from multiple matings in terms of increased lifetime offspring production. Despite a negative effect of remating on female longevity in species without nuptial feeding, the positive effects (increased egg production rate and fertility) more than outweigh this negative effect for moderate mating rates. The average direct net fitness gain of multiple mating was as high as 30-70%. Therefore, the evolutionary maintenance of polyandry in insects can be understood solely in terms of direct effects. However, our results also strongly support the existence of an intermediate optimal female mating rate, beyond which a further elevated mating rate is deleterious. The existence of such optima implies that sexual conflict over the mating rate should be very common in insects, and that sexually antagonistic coevolution plays a key role in the evolution of mating systems and of many reproductive traits. We discuss the origin and maintenance of nuptial feeing in the light of our findings, and suggest that elaborate and nutritional ejaculates may be the result of sexually antagonistic coevolution. Future research should aim at gaining a quantitative understanding of the evolution of female mating rates. Copyright 2000 The Association for the Study of Animal Behaviour.

Journal Article↗

Effects of host sociality on ectoparasite population biology.

Theory predicts a positive relationship between parasite infection intensity and host density. However, this generalization is complicated in natural systems by differences in life history among parasite taxa, e.g., transmissibility. Accordingly, predictions relating host density to parasite load should be specific to each parasite taxon. To illustrate this, we studied parasites that differed greatly in life history in the context of the Galapagos hawk's (Buteo galapagoensis) variably cooperative mating system. Two louse (Phthiraptera) species were collected: Colpocephalum turbinatum (Amblycera), with 53 host species, and Degeeriella regalis (Ischnocera), with 10 host species, although B. galapagoensis was the only known Galapagos host. Sixty territorial adult male hawks from 26 groups of 1-6 males were quantitatively sampled for lice. Average abundance and intensity of C. turbinatum but not D. regalis were significantly larger in large groups of hawks than small groups. Males from the same polyandrous group harbored significantly correlated abundances of C. turbinatum but not D. regalis. Prevalence, average abundance, and intensity of C. turbinatum were significantly higher than D. regalis. These are the first results to demonstrate significant differences in a suite of population responses between these louse suborders in the context of host sociality.

Animals↗

Intraspecific variation in the induction of female sexual receptivity in prairie voles.

Prairie voles (Microtus ochrogaster) are monogamous New World rodents which show geographic variation in social behavior. In this study, parameters of female reproduction which might be related to mating system were compared in prairie voles from eastern Kansas (KAN) versus central Illinois (ILL). KAN females showed a more rapid onset of natural estrus following exposure to a male and were more likely to respond to injections of a low dose (0.5 microg) of exogenous estradiol benzoate than ILL females. Neither mating duration nor pregnancy success after mate removal differed in KAN versus ILL females. These results suggest that ILL voles are less sensitive than KAN voles to the estrus-inducing effects of either endogenous or exogenous estrogen, supporting the hypothesis that variations in reproductive strategy occur among geographically discrete populations of prairie voles.

Animals↗

Individual variation in inbreeding depression: the roles of inbreeding history and mutation.

We use mutation-selection recursion models to evaluate the relative contributions of mutation and inbreeding history to variation among individuals in inbreeding depression and the ability of experiments to detect associations between individual inbreeding depression and mating system genotypes within populations. Poisson mutation to deleterious additive or recessive alleles generally produces far more variation among individuals in inbreeding depression than variation in history of inbreeding, regardless of selfing rate. Moreover, variation in inbreeding depression can be higher in a completely outcrossing or selfing population than in a mixed-mating population. In an initially random mating population, the spread of a dominant selfing modifier with no pleiotropic effects on male outcross success causes a measurable increase in inbreeding depression variation if its selfing rate is large and inbreeding depression is caused by recessive lethals. This increase is observable during a short period as the modifier spreads rapidly to fixation. If the modifier alters selfing rate only slightly, it fails to spread or causes no measurable increase in inbreeding depression variance. These results suggest that genetic associations between mating loci and inbreeding depression loci could be difficult to demonstrate within populations and observable only transiently during rapid evolution to a substantially new selfing rate.

Animals↗

Genetic structure among closely spaced leks in a peripheral population of lesser prairie-chickens.

We evaluated the genetic structure of birds from four closely spaced leks in a peripheral population of lesser prairie-chickens (Tympanuchus pallidicinctus). Analyses of molecular variance revealed significant genetic structuring among birds from different leks for six microsatellite loci (FST = 0.036; P = 0.002), but we found no genetic differentiation at the mtDNA control region. Significant deviations from Hardy-Weinberg revealed an excess of homozygote genotypes within each of the leks studied (FIS = 0.190-0.307), indicative of increased inbreeding. Estimates of relatedness using microsatellite data suggest that the genetic structuring among lesser prairie-chicken leks occurs in part because of a lek mating system in which males at some leks are related. Structuring may also be caused by stochastic effects associated with a historical decline in population size leading to small, semi-isolated leks and high site fidelity by reproductive males. Results from this study suggest that microspatial genetic structuring may occur in lek-mating bird species with low levels of dispersal.

Analysis of Variance↗

Structure-activity relationships of the yeast alpha-factor.

The yeast Saccharomyces cerevisiae produces a peptide pheromone, termed the alpha-factor, as a prelude to sexual conjugation. Haploid MAT alpha-cells, but not haploid MAT a-cells or MAT a/alpha-diploids, produce this tridecapeptide of the structure: Trp-His-Trp-Leu-Gln-Leu-Lys-Pro-Gly-Gln-Pro-Met-Tyr. Structural analogues of the alpha-factor have been prepared with alterations in many of the residues, derivatized peptides have been synthesized, and truncated and elongated peptides have been studied. These peptides have been analyzed for their biological activities by various assays. Mutants of S. cerevisiae have been isolated that do not respond to alpha-factor or are supersensitive to the pheromone and its analogues. The mating system of S. cerevisiae provides a powerful model in which genetics, biochemistry, and molecular biology can be used to unravel the mysteries of peptide hormone structure and function.

Amino Acid Sequence↗

Variance of actual inbreeding.

The variances of actual inbreeding and coancestry in terms of their corresponding identities by descent were studied for finite populations. For inbreeding at a single locus, the total variance sigma 2 equal F(1-F) (F is the inbreeding coefficient) is comprised of a component sigma 2w within populations and a component sigma 2b between replicate populations. These variances increase in time to a maximum at about 1.1Ne generations for sigma 2w, about 2.3Ne generations for sigma 2b, and about 1.4 NE generations for sigma 2, and decrease thereafter (Ne is effective population size). The ratio sigma 2b/sigma 2 is ever increasing to an asymptote in the range 0.4-0.5 depending on Ne and the mating system. For finite populations with variation in pedigree F's, there are contributions sigma 2wF within and sigma 2bF between populations. The component sigma 2bF is insignificant except for very small populations, and sigma 2wF is largest in the early generations and then decreases roughly as (1-F)2/KNe where K is formulated in terms of the mating strategy and the degree of avoidance of mating relatives. An additional degree of avoidance increases K by a factor of 4. In a large population at equilibrium with respect to mixed self and random mating, sigma 2wF accounts for one-half to two-thirds of sigma 2w. Bringing in more loci leads to decomposition of the total variance into four components whose values are affected by linkages among the loci. The relationships between these components and sigma 2w, sigma 2wF, and sigma 2bF are elaborated in terms of tight and loose linkage. The exact computations of sigma 2wF and sigma 2bF require the use of two locus descent measures without linkage. The variances of various averages of actual identities by descent, such as the proportions for individuals or populations, are formulated for a sample of individuals.

Analysis of Variance↗

Sex pheromones of two Asian moths (Creatonotos transiens, C. gangis; Lepidoptera--Arctiidae): behavior, morphology, chemistry and electrophysiology.

Two sympatric species of Asian arctiid moths (Creatonotos spp.) use a sequential, dual luring and mating system. After sunset males pneumatically expand their coremata from a cavity between the abdominal sternites 7 and 8 and release their pheromone. They attract other males and thus, scent-emitting male groups may develop. About 30 min later females are attracted to the calling males. Upon contact with a female the male's corema deflates and mating follows. After 1-2 h the male calling subsides and now the remaining virgin females continue to emit their pheromone bouquet from internal, tubular glands located in the dorsal part of the abdomen, rostrad from tergite 8/9. This attracts males and further matings occur.- The coremata are huge, pneumatically eversible organs composed of two pairs of tubes, up to 37 mm long, each covered by ca. 3000 scent hairs (scales). There is a giant epidermal (trichogen) gland cell at the base of each hair. One large corema may contain up to 0.5 mg of the pheromone, hydroxydanaidal. The internal, tubular female glands are antler shaped; their air-filled lumen is ventilated by abdominal pumping. The major components of the female attractant are (Z,Z,Z)-3,6,9-heneicosatriene and (Z,Z)-2 (2,5-octadienyl)-3-undecyloxirane with different ratios in the two species. One of the minor components, common to both species, is (Z,Z,Z)-3,6,9-tricosatriene. Only the male antennae possess specialized receptor cells for the female attractants; other antennal cells of both sexes respond to the male pheromone.

Animals↗

Reproductive performance and estimates of labor requirements associated with combinations of artificial insemination and natural service in swine.

A study was conducted to examine effects of mating systems composed of natural service (NS) and AI in swine on farrowing rate, litter size, and labor requirements. Sows and gilts were bred once per day via one of the following treatments (d 1/d 2): NS/NS, NS/AI, AI/AI, and NS/none. Gilts bred with NS/AI, AI/AI, and NS/NS had higher (P less than .05) farrowing rates than gilts bred with NS/none matings. Similarly, farrowing rates were higher (P less than .05) in NS/AI than in NS/NS gilts. Numbers of pigs born alive were greater (P less than .05) in NS/NS, NS/AI, and AI/AI than in NS/none gilts. In sows, a treatment x time interaction (P less than .01) was present for farrowing rate. In the AI/AI treatment, farrowing rate increased (P less than .01) from 70.0% (wk 1 through 3) to 88.5% (wk 4 through 10). Farrowing rates were 87.3, 93.2, and 76.0% in the NS/NS, NS/AI, and NS/none groups, respectively, and did not change (P = .72) over time. Sows bred via NS/NS and NS/AI had larger litters (P less than .05) than NS/none sows. In the present study, if four or more sows and gilts were bred, then AI required less (P less than .05) time per animal than NS. Furthermore, gilts required more (P less than .05) time for breeding than sows. Results from this study demonstrate that gilts and sows responded differently to combinations of NS and AI in terms of reproductive performance. In addition, differences in labor requirements per sow or gilt between NS and AI matings were dependent on parity and daily breeding demands.

Age Factors↗

Physiological suppression of sexual function of subordinate males: a subtle form of intrasexual competition among male sifakas (Propithecus verreauxi)?

In contrast to most anthropoid primates, sifakas (Propithecus verreauxi), like many group-living lemurs, exhibit a number of features that deviate from predictions of sexual selection theory. Despite a promiscuous mating system, they lack sexual dimorphism, suggesting that physical combat plays only a minor role in intrasexual competition for receptive females. In this study, we investigated the hypothesis that socioendocrinological mechanisms contribute to suppression of reproductive function of subordinate males. For that purpose, 10 male sifakas from five social groups were observed for 669 focal animal hours for 4 months, including the mating season, in Western Madagascar. Concomitantly 315 fecal samples of these animals were collected and the concentration of immunoreactive testosterone was quantified hy enzymeimmunoassay procedures. Clear dominance relationships existed among coresident males. Testosterone levels of dominant males were significantly higher than those of subordinates during, as well as outside, the mating season. Additionally, the increase in testosterone levels prior to the mating season was more pronounced for dominant than for subordinate males. These findings are in accordance with the hypothesis of suppression of sexual function of subordinate males, probably providing dominant males with ani advantage in sperm competition. If reproductive success is mainly determined by this nonagonistic form of intrasexual competition, the results of this study contribute an important piece to the puzzle of lacking sexual dimorphism in P. verreauxi.

Adaptation, Physiological↗

The advantage of factorial mating under selection is uncovered by deterministically predicted rates of inbreeding.

Rates of inbreeding (DeltaF) in selected populations were predicted using the framework of long-term genetic contributions and validated against stochastic simulations. Deterministic predictions decomposed DeltaF into four components due to: finite population size, directional selection, covariance of genetic contribution of mates, and deviation of variance of family size from that expected from a Poisson distribution. Factorial (FM) and hierarchical (HM) mating systems were compared under mass and sib-index selection. Prediction errors were in most cases for DeltaF less than 10% and for rate of gain less than 5%. DelatF was higher with index than mass selection. DeltaF was lower with FM than HM in all cases except random selection. FM reduced the variance of the average breeding value of the mates of an individual. This reduced the impact of the covariance of contributions of mates on DeltaF. Thus, contributions of mates were less correlated with FM than HM, causing smaller deviations of converged contributions from the optimum contributions. With index selection, FM also caused a smaller variance of number of offspring selected from each parent. This reduced variance of family size reduced DeltaF further. FM increases the flexibility in breeding schemes for achieving the optimum genetic contributions.

Animals↗

Female preference for fly song: playback experiments confirm the targets of sexual selection.

The courtship song of Drosophila is thought to be involved in sexual selection and species recognition. Because of the mating system of flies, however, directly demonstrating that song influences female preference is difficult. The majority of previous studies have used an experimental design that potentially confounds male and female reactions to song. In D. montana, correlational evidence has suggested that males that produce short sound pulses consisting of a high number of sound cycles (i.e. a high carrier frequency) have a higher mating success than other males. In this study, we played synthetic song that varied in pulse length and carrier frequency to individual females in the laboratory, both alone and in the presence of mute males. We scored female preference via an acceptance posture, 'wing spreading', which the females of this species usually display prior to mounting by a male. Females responded to synthetic song in the absence of males. The presence of mute males significantly increased their overall responsiveness, but the relative effectiveness of the songs did not change, eliminating male reaction to song as a possible confounding factor in the results. The interaction between pulse length and carrier frequency determined the discrimination between song types, with females responding most readily to song consisting of short pulses with a high carrier frequency. Thus, direct examination of female preferences supports the previous studies of male mating success, and confirms female song preference as a likely determinant of male mating success. Copyright 1998 The Association for the Study of Animal Behaviour

Journal Article↗

Is male-infant caretaking related to paternity and/or mating activities in wild Barbary macaques (Macaca sylvanus)?

In species with a promiscuous mating system, the functions of male-infant caretaking remain unclear in the absence of genetic paternity tests. We tested paternal investment and hypotheses concerning reproductive tactics in wild groups of Barbary macaques, including results of genetic paternity tests. Our study revealed that male-infant caretaking was not related to the probability of paternity. In principle, males could use access to females to estimate paternity. However, we found that mating success was not related to paternity, so males could invest in infants that they had not sired, and caretaking of non-offspring was actually observed. Accordingly, males might be 'deceived' with respect to their paternal investment. In that case, one would expect a positive relation between mating success and the subsequent rate of male caretaking of infants. Such a relation is also lacking, leading to comprehensive rejection of the paternal investment hypothesis in Barbary macaques. By contrast, there was evidence that males showing infant care achieved higher mating frequencies than other males with the mothers of the relevant infants. Thus, male Barbary macaques do not show a 'mate-then-care' pattern, but they do exhibit a 'care-then-mate' pattern.

Animals↗

Spatial population genetic structure in Trillium grandiflorum: the roles of dispersal, mating, history, and selection.

The roles of the various potential ecological and evolutionary causes of spatial population genetic structure (SPGS) cannot in general be inferred from the extant structure alone. However, a stage-specific analysis can provide clues as to the causes of SPGS. We conducted a stage-specific SPGS analysis of a mapped population of about 2000 Trillium grandiflorum (Liliaceae), a long-lived perennial herb. We compared SPGS for juvenile (J), nonreproductive (NR), and reproductive (R) stages. Fisher's exact test showed that genotypes had Hardy-Weinberg frequencies at all loci and stage classes. Allele frequencies did not differ between stages. Bootstrapped 99% confidence intervals (99%CI) indicate that F-statistic values are indistinguishable from zero, (except for a slightly negative FIT for the R stage). Spatial autocorrelation was used to calculate f the average kinship coefficient between individuals within distance intervals. Null hypothesis 99%CIs for f were constructed by repeatedly randomizing genotypic locations. Significant positive fine-scale genetic structure was detected in the R and NR stages, but not in the J stage. This structure was most pronounced in the R stage, and declined by about half in each remaining stage: near-neighbor f = 0.122, 0.065, 0.027, for R, NR, and J, respectively. For R and NR, the near-neighbor f lies outside the null hypothesis 99%CI, indicating kinship at approximately the level of half-sibs and first cousins, respectively. We also simulated the expected SPGS of juveniles post dispersal, based on measured R-stage SPGS, the mating system, and measured pollen and seed dispersal properties. This provides a null hypothesis expectation (as a 99%CI) for the J-stage correlogram, against which to test the likelihood that post-dispersal events have influenced J-stage SPGS. The actual J correlogram lies within the null hypothesis 99%CI for the shortest distance interval and nearly all other distance intervals indicating that the observed low recruitment, random mating and seed dispersal patterns are sufficient to account for the disappearance of SPSG between the R and the J stages. The observed increase in SPGS between J and R stages has two potential explanations: history and local selection. The observed low total allelic diversity is consistent with a past bottleneck: a possible historical explanation. Only a longitudinal stage-specific study of SPGS structure can distinguish between historical events and local selection as causes of increased structure with increasing life history stage.

Genetics, Population↗

Male phenotype predicts insemination success in guppies.

Theory predicts that mate choice can lead to an increase in female fecundity if the secondary sexual traits used by females to assess male quality covary with the number of sperm transferred during copulation. Where females mate multiply, such a relationship between male attractiveness and ejaculate size may, additionally (or alternatively), serve to augment the effect of indirect selection by biasing paternity in favour of preferred males. In either case, a positive correlation between male attractiveness and the size of ejaculates delivered at copulation is predicted. To date, some of the most convincing (indirect) evidence for this prediction comes from the guppy, a species of fish exhibiting a resource-free mating system in which attractive males tend to have larger sperm reserves. We show that, during solicited copulations, male guppies with preferred phenotypes actually transfer more sperm to females than their less-ornamented counterparts, irrespective of the size of their initial sperm stores. Our results also reveal that, during coercive copulations, the relationship between ejaculate size and the male's phenotype breaks down. This latter result, in conjunction with our finding that mating speed--a factor under the female's control-is a significant predictor of ejaculate size, leads us to speculate that females may exert at least partial control over the number of sperm inseminated during cooperative matings.

Animals↗

Unrelated helpers in a social insect.

High-resolution genetic markers have revolutionized our understanding of vertebrate mating systems, but have so far yielded few comparable surprises about kinship in social insects. Here we use microsatellite markers to reveal an unexpected and unique social system in what is probably the best-studied social wasp, Polistes dominulus. Social insect colonies are nearly always composed of close relatives; therefore, non-reproductive helping behaviour can be favoured by kin selection, because the helpers aid reproductives who share their genes. In P. dominulus, however, 35% of foundress nestmates are unrelated and gain no such advantage. The P. dominulus system is unlike all other cases of unrelated social insects, because one individual has nearly complete reproductive dominance over subordinates who could have chosen other reproductive options. The only significant advantage that subordinates obtain is a chance at later reproduction, particularly if the queen dies. Thus, P. dominulus societies are functionally unlike other social insects, but similar to certain vertebrate societies, in which the unrelated helpers gain through inheritance of a territory or a mate.

Animals↗

Simulation of cow-calf production systems in a range environment: II. Model evaluation.

Development of a general beef cattle simulation model was described in a companion paper. The objectives of this research were to demonstrate and evaluate the model's performance. Four experiments were conducted to demonstrate 1) life-cycle weight and body condition changes for different genotypes raised in a northern range environment; 2) responses in forage intake and weight to changes in forage quality, protein supplementation, and cow physiological state; 3) responses in reproduction, weight, body condition, and calf growth to differences in pre- and postpartum nutrition; and 4) differences in enterprise efficiency and profit for different genotypes and mating systems. Results indicated that the model performs acceptably for the types of situations for which it was designed and highlighted areas of animal science where more information is needed in order to better understand and manipulate beef cattle systems. Computer simulation models are useful tools to facilitate the integration of scientific concepts and to help scientists, teachers, and producers better understand the complex production systems that they study and manage. In addition to addressing enterprise-level problems that are beyond the scope of traditional experimentation, modeling and simulation help identify research needs and foster exchange among disciplines.

Animal Feed↗

Sexual selection resulting from extrapair paternity in collared flycatchers.

Extrapair paternity has been suggested to represent a potentially important source of sexual selection on male secondary sexual characters, particularly in birds with predominantly socially monogamous mating systems. However, relatively few studies have demonstrated sexual selection within single species by this mechanism, and there have been few attempts to assess the importance of extrapair paternity in relation to other mechanisms of sexual selection. We report estimates of sexual selection gradients on male secondary sexual plumage characters resulting from extrapair paternity in the collared flycatcher Ficedula albicollis, and compare the importance of this form of sexual selection with that resulting from variation in mate fecundity. Microsatellite genotyping revealed that 15% of nestlings, distributed nonrandomly among 33% of broods (N=79), were the result of extrapair copulations. Multivariate selection analyses revealed significant positive directional sexual selection on two uncorrelated secondary sexual characters in males (forehead and wing patch size) when fledgling number was used as the measure of fitness. When number of offspring recruiting to the breeding population was used as the measure of male fitness, selection on these traits appeared to be directional and stabilizing, respectively. Pairwise comparisons of cuckolded and cuckolding males revealed that males that sired young through extrapair copulations had wider forehead patches, and were paired to females that bred earlier, than the males that they cuckolded. Path analysis was used to partition selection on these traits into pathways via mate fecundity and sperm competition, and suggested that the sperm competition pathway accounted for between 64 and 90% of the total sexual selection via the two paths. The selection revealed in these analyses is relatively weak in comparison with many other measures of selection in natural populations. We offer some explanations for the relatively weak selection detected. Copyright 1999 The Association for the Study of Animal Behaviour.

Journal Article↗