Selection for costly sexual traits results in a vacant mating niche and male dimorphism

The expected strong directional selection for traits that increase a male's mating ability conflicts with the frequent observation that within species, males may show extreme variation in sexual traits. These male reproductive polymorphisms are usually attributed to direct male–male competition. It is currently unclear, however, how directional selection for sexually selected traits may convert into disruptive selection, and if female preference for elaborate traits may be an alternative mechanism driving the evolution of male polymorphism. Here, we explore this mechanism using the polyandric dwarf spider Oedothorax gibbosus as a model. We first show that males characterized by conspicuous cephalic structures serving as a nuptial feeding device (“gibbosus males”) significantly outperform other males in siring offspring of previously fertilized females. However, significant costs in terms of development time of gibbosus males open a mating niche for an alternative male type lacking expensive secondary sexual traits. These “tuberosus males” obtain virtually all fertilizations early in the breeding season. Individual‐based simulations demonstrate a hitherto unknown general principle, by which males selected for high investment to attract females suffer constrained mating opportunities. This creates a vacant mating niche of unmated females for noninvesting males and, consequently, disruptive selection on male secondary sexual traits.     

Size‐dependent reproductive success of wild zebrafish Danio rerio in the laboratory

Size‐dependent reproductive success of wild zebrafish Danio rerio was studied under controlled conditions in the laboratory to further understand the influence of spawner body size on reproductive output and egg and larval traits. Three different spawner size categories attained by size‐selective harvesting of the F₁‐offspring of wild D. rerio were established and their reproductive performance compared during a 5 day period. As to be expected, large females spawned more frequently and had significantly greater clutch sizes than small females. Contrary to expectations, small females produced larger eggs when measured as egg diameter with similar amounts of yolk compared to eggs spawned by large spawners. Eggs from small fish, however, suffered from higher egg mortality than the eggs of large individuals. Embryos from small‐sized spawners also hatched later than offspring from eggs laid by large females. Larval standard length (L_S)‐at‐hatch did not differ between the size categories, but the offspring of the large fish had significantly larger area‐at‐hatch and greater yolk‐sac volume indicating better condition. Offspring growth rates were generally similar between offspring from all size categories, but they were significantly higher for offspring spawned by small females in terms of L_S between days 60 and 90 post‐fertilization. Despite temporarily higher growth rates among the small fish offspring, the smaller energy reserves at hatching translated into lower condition later in ontogeny. It appeared that the influence of spawner body size on egg and larval traits was relatively pronounced early in development and seemed to remain in terms of condition, but not in growth, after the onset of exogenous feeding. Further studies are needed to explore the mechanisms behind the differences in offspring quality between large‐ and small‐sized spawners by disentangling size‐dependent maternal and paternal effects on reproductive variables in D. rerio.     

Various X2-Tests of Homogeneity: Some Comments

Methodological issues in the analysis of incidence rates or prevalence proportions for count data, presented in a form of a sequence of 2×2 tables, corresponding to levels (strata) of a specified variable (risk factor) X, are discussed. Suppose λ_1i and λ_2i are the incidence rates of an event D in the ith stratum for populations 1 and 2, respectively. The homogeneity (null) hypothesis is formulated in the form: H_0:λ1i=λ_2i for all i (i = 1, 2, …, I). Three X²-tests for H₀ and their theoretical bases are discussed: X_Total² which is sensitive to alternatives HA :λ1i± λ2i for at least some i; X_Comb² which is sensitive to alternatives H A : λ1iλ2i² or < λ_2i but not both for all i; and X_Diff² which is sensitive to alternatives H_A:λ1i>λ2i³ for some i and λ_1i′ < λ_2i′ for some i′ (i≠i′). These statistics satisfy the relation X_Total² = X_Comb² + X_Diff². Also, X′²-statistic for pooled data is calculated, which in conjunction with X_Comb² can serve for detecting confounding. Although most of these techniques are known, they are rather scattered in the literature, and not always considered jointly, as it is emphasized in the present paper. It is hoped that these comments will be helpful to biostatisticians as well as to epidemiologists and medical researchers in the analysis of mortality and morbidity data. For illustration, two examples with large sets of epidemiological data are given.     

Male phenotypes in a female framework: Evidence for degeneration in sperm produced by male snails from asexual lineages

How changes in selective regimes affect trait evolution is an important open biological question. We take advantage of naturally occurring and repeated transitions from sexual to asexual reproduction in a New Zealand freshwater snail species, Potamopyrgus antipodarum, to address how evolution in an asexual context—including the potential for relaxed selection on male‐specific traits—influences sperm morphology. The occasional production of male offspring by the otherwise all‐female asexual P. antipodarum lineages affords a unique and powerful opportunity to assess the fate of sperm traits in a context where males are exceedingly rare. These comparisons revealed that the sperm produced by ‘asexual’ males are markedly distinct from sexual counterparts. We also found that the asexual male sperm harboured markedly higher phenotypic variation and was much more likely to be morphologically abnormal. Together, these data suggest that transitions to asexual reproduction might be irreversible, at least in part because male function is likely to be compromised. These results are also consistent with a scenario where relaxed selection and/or mutation accumulation in the absence of sex translates into rapid trait degeneration.     

Determinants and long‐term costs of early reproduction in males of a long‐lived polygynous mammal

In long‐lived polygynous species, male reproductive success is often monopolized by a few mature dominant individuals. Young males are generally too small to be dominant and may employ alternative tactics; however, little is known about the determinants of reproductive success for young males. Understanding the causes and consequences of variability in early reproductive success may be crucial to assess the strength of sexual selection and possible long‐term trade‐offs among life‐history traits. Selective pressures driven by fluctuating environmental conditions may depend on age class. We evaluated the determinants of reproduction in male bighorn sheep (Ovis canadensis) aged 2–4 years using 30 years of individual‐level data. These young males cannot defend estrous ewes and use alternative mating tactics. We also investigated how the age of first detected reproduction was correlated to lifetime reproductive success and longevity. We found that reproductive success of males aged 3 years was positively correlated to body mass, to the proportion of males aged 2–4 years in the competitor pool, and to the number of females available per adult male. These results suggest that reproductive success depends on both competitive ability and population age–sex structure. None of these variables, however, had significant effects on the reproductive success of males aged 2 or 4 years. Known reproduction before the age of five increased lifetime reproductive success but decreased longevity, suggesting a long‐term survival cost of early reproduction. Our analyses reveal that both individual‐level phenotypic and population‐level demographic variables influence reproductive success by young males and provide a rare assessment of fitness trade‐offs in wild polygynous males.     

A functional trait approach to identifying life history patterns in stochastic environments

Temporal variation in demographic processes can greatly impact population dynamics. Perturbations of statistical coefficients that describe demographic rates within matrix models have, for example, revealed that stochastic population growth rates (log(λ_s)) of fast life histories are more sensitive to temporal autocorrelation of environmental conditions than those of slow life histories. Yet, we know little about the mechanisms that drive such patterns. Here, we used a mechanistic, functional trait approach to examine the functional pathways by which a typical fast life history species, the macrodetrivore Orchestia gammarellus, and a typical slow life history species, the reef manta ray Manta alfredi, differ in their sensitivity to environmental autocorrelation if (a) growth and reproduction are described mechanistically by functional traits that adhere to the principle of energy conservation, and if (b) demographic variation is determined by temporal autocorrelation in food conditions. Opposite to previous findings, we found that O. gammarellus log(λ_s) was most sensitive to the frequency of good food conditions, likely because reproduction traits, which directly impact population growth, were most influential to log(λ_s). Manta alfredi log(λ_s) was instead most sensitive to temporal autocorrelation, likely because growth parameters, which impact population growth indirectly, were most influential to log(λ_s). This differential sensitivity to functional traits likely also explains why we found that O. gammarellus mean body size decreased (due to increased reproduction) but M. alfredi mean body size increased (due to increased individual growth) as food conditions became more favorable. Increasing demographic stochasticity under constant food conditions decreased O. gammarellus mean body size and increased log(λ_s) due to increased reproduction, whereas M. alfredi mean body and log(λ_s) decreased, likely due to decreased individual growth. Our findings signify the importance of integrating functional traits into demographic models as this provides mechanistic understanding of how environmental and demographic stochasticity affects population dynamics in stochastic environments.     

Predicting evolutionary responses to selection on polyandry in the wild: additive genetic covariances with female extra-pair reproduction

The evolutionary forces that underlie polyandry, including extra-pair reproduction (EPR) by socially monogamous females, remain unclear. Selection on EPR and resulting evolution have rarely been explicitly estimated or predicted in wild populations, and evolutionary predictions are vulnerable to bias due to environmental covariances and correlated selection through unmeasured traits. However, evolutionary responses to (correlated) selection on any trait can be directly predicted as additive genetic covariances (cov_A) with appropriate components of relative fitness. I used comprehensive life-history, paternity and pedigree data from song sparrows (Melospiza melodia) to estimate cov_A between a female''s liability to produce extra-pair offspring and two specific fitness components: relative annual reproductive success (ARS) and survival to recruitment. All three traits showed non-zero additive genetic variance. Estimates of cov_A were positive, predicting evolution towards increased EPR, but 95% credible intervals overlapped zero. There was therefore no conclusive prediction of evolutionary change in EPR due to (correlated) selection through female ARS or recruitment. Negative environmental covariance between EPR and ARS would have impeded evolutionary prediction from phenotypic selection differentials. These analyses demonstrate an explicit quantitative genetic approach to predicting evolutionary responses to components of (correlated) selection on EPR that should be unbiased by environmental covariances and unmeasured traits.     

Small‐scale spatial variation in evolvability for life‐history traits in the storm petrel

The evolutionary potential in the timing of recruitment and reproduction may be crucial for the ability of populations to buffer against environmental changes, allowing them to avoid unfavourable breeding conditions. The evolution of a trait in a local population is determined by its heritability and selection. In the present study, we performed pedigree‐based quantitative genetic analyses for two life‐history traits (recruiting age and laying date) using population data of the storm petrel over an 18‐year period in two adjacent breeding colonies (only 150 m apart) that share the same environmental conditions. In both traits, natal colony effect was the main source of the phenotypic variation among individuals, and cohort variance for recruitment age and additive genetic variance for laying date were natal colony‐specific. We found significant heritability only in laying date and, more specifically, only in birds born in one of the colonies. The difference in genetic variance between the colonies was statistically significant. Interestingly, selection on earlier breeding birds was detected only in the colony in which heritable variation in laying date was found. Therefore, local evolvability for a life‐history trait may vary within a unexpectedly small spatial scale, through the diversifying natural selection and insulating gene flow. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106 , 439–446.     

Predators modify the temperature dependence of life‐history trade‐offs

Although life histories are shaped by temperature and predation, their joint influence on the interdependence of life‐history traits is poorly understood. Shifts in one life‐history trait often necessitate shifts in another—structured in some cases by trade‐offs—leading to differing life‐history strategies among environments. The offspring size–number trade‐off connects three traits whereby a constant reproductive allocation (R) constrains how the number (O) and size (S) of offspring change. Increasing temperature and size‐independent predation decrease size at and time to reproduction which can lower R through reduced time for resource accrual or size‐constrained fecundity. We investigated how O, S, and R in a clonal population of Daphnia magna change across their first three clutches with temperature and size‐independent predation risk. Early in ontogeny, increased temperature moved O and S along a trade‐off curve (constant R) toward fewer larger offspring. Later in ontogeny, increased temperature reduced R in the no‐predator treatment through disproportionate decreases in O relative to S. In the predation treatment, R likewise decreased at warmer temperatures but to a lesser degree and more readily traded off S for O whereby the third clutch showed a constant allocation strategy of O versus S with decreasing R. Ontogenetic shifts in S and O rotated in a counterclockwise fashion as temperature increased and more drastically under risk of predation. These results show that predation risk can alter the temperature dependence of traits and their interactions through trade‐offs.     

Geographical and seasonal variation in the intensity of sexual selection in the barn swallow Hirundo rustica: a meta‐analysis

Sexual selection arises from competition among individuals for access to mates, resulting in the evolution of conspicuous sexually selected traits, especially when inter‐sexual competition is mediated by mate choice. Different sexual selection regimes may occur among populations/subspecies within the same species. This is particularly the case when mate choice is based on multiple sexually selected traits. However, empirical evidence supporting this hypothesis at the among‐populations level is scarce. We conducted a meta‐analysis of the intensity of sexual selection on the largest database to date for a single species, the barn swallow (Hirundo rustica), relying on quantitative estimates of sexual selection. The intensity of sexual selection was expressed as the strength (effect size) of the relationships between six plumage ornaments (tail length, tail asymmetry, size of white spots on tail, ventral plumage colour, throat plumage colour and throat patch size) and several fitness proxies related to reproduction, parental care, offspring quality, arrival date from spring migration, and survival. The data were gathered for four geographically separated subspecies (H. r. rustica, H. r. erythrogaster, H. r. gutturalis, H. r. transitiva). The overall mean effect size (Z_r = 0.214; 95% confidence interval = 0.175–0.254; N = 329) was of intermediate magnitude, with intensity of sexual selection being stronger in males than in females. Effect sizes varied during the breeding cycle, being larger before egg deposition, when competition for access to mates reaches its maximum (i.e. in the promiscuous part of the breeding cycle), and decreasing thereafter. In addition, effect sizes from experiments were not significantly larger than those from correlative studies. Finally, sexual selection on different sexually dimorphic traits varied among subspecies. This last result suggests that morphological divergence among populations has partly arisen from divergent sexual selection, which may eventually lead to speciation.     

BREEDING RESOURCE DISTRIBUTION AFFECTS SELECTION GRADIENTS ON MALE PHENOTYPIC TRAITS: EXPERIMENTAL STUDY ON LIFETIME REPRODUCTIVE SUCCESS IN THE BITTERLING FISH (RHODEUS AMARUS)

The spatial distribution of breeding resources can have pronounced demographic and evolutionary consequences. We used 20 experimental groups of the bitterling ( Rhodeus amarus ), an annual fish with a promiscuous, resource-based mating system, and extended breeding season to investigate how the spatial distribution (clumped or regular) of bitterling oviposition sites (live freshwater mussels) affected offspring production, variation in reproductive success, and directional selection on phenotypic traits over their entire reproductive lifetime. We did not detect any effect of resource distribution on offspring production or variation in reproductive success among individual fish, although variation between replicates was higher with a clumped distribution. This finding is discussed with regard to the incidence of alternative mating behaviors (sneaking) within the limitations imposed by our experimental design. Breeding resource distribution had a significant effect on selection on male phenotypic traits. Stronger directional selection on traits associated with intrasexual competition for fertilizations, gonad mass (an indicator of sperm competition), and the extent of red, carotenoid-based pigment in the iris (an index of dominance status), was detected with a clumped resource distribution. With a regular resource distribution, a stronger positive selection on male body size was detected. We discuss the implications of our results for natural populations.     

The short-term and long-term effects of parental age in the bean weevil (Acanthoscelides obtectus)

We examined the influence of parental age on life history traits of their offspring in the lines of bean weevil that have evolved different rates of senescence. Measurements included preadult traits (egg size, embryonic developmental time, total preadult developmental time, preadult viability) and adult traits (body weight, total realized fecundity of females, first day of egg laying, early fecundity, late fecundity and longevity). The negative parental age effects were observed for all traits except for the early and total realized fecundity. We did not detect statistically significant line×parental age interactions for either preadult- or adult-survival, so offspring survival did not change with parental age after selection for early vs. late reproduction. It seems that selection acting on the quality of offspring produced by parents of different ages has not been responsible for the evolution of senescence in bean weevil. This revised version was published online in August 2006 with corrections to the Cover Date.     

Identification of agronomically favorable quantitative trait loci alleles from a dent corn inbred Dan232 using advanced backcross QTL analysis and comparison with the F<Subscript>2:3</Subscript> population in popcorn

Specific traits are an important consideration in plant breeding. In popcorn, inferior agronomic traits could be improved using dent or flint corn backcrossed with popcorn. In this study, we used advanced backcross quantitative trait locus (AB-QTL) analysis to identify trait-improving QTL alleles from a dent maize inbred Dan232, and compared the detection of QTL in the BC₂S₁ population with QTL results using F_2:3 families of the same population. Two hundred and twenty BC₂S₁ families developed from a cross between Dan232 and an elite popcorn inbred N04 were evaluated for nine plant traits in replicated field trials under two environments. Using composite interval mapping (CIM), a total of 28 significant QTL were detected, and of these, 23 (82.14%) had favorable alleles contributed by the dent corn parent Dan232. Nine QTL (32.14%) detected in the BC₂S₁ population were also located in or near the same chromosome intervals in the F_2:3 population. All of the favorable QTL alleles from Dan232 could be used in marker-assisted selection (MAS) to improve the respective plant traits in popcorn breeding. In addition, their near isogenic lines (QTL-NILs) could be obtained through selfing or another 1–2 backcross with N04. Also, N04 improved for the studied plant traits could be developed from the BC₂S₁ families used in this study. This study demonstrated that the AB-QTL method can be applied to identify favorable QTL from dent corn inbred in popcorn breeding and, once identified, the alleles could be used in marker-assisted selection to improve the respective plant traits.     

Resistance in tomato to the greenhouse whitefly: analysis of population dynamics

Life history parameters including longevity, developmental time, and reproduction were determined for whiteflies, Trialeurodes vaporariorum (Westwood), kept in clip-on cages on susceptible parent, Lycopersicon esculentum, resistant parent, L. hirsutum glabratum, and intermediate breeding lines of tomato. Using the Lewontin triangular reproductive function, the intrinsic rate of increase (r_m) was calculated for each genotype. This is an elegant tool for detecting resistance, as it incorporates all salient factors of life history. Comparing r_m to the other parameters measured, selection criteria were chosen. Developmental time is not a suitable selection criterion as it varies very little even between the most susceptible and the most resistant genotypes. Additionally, developmental time of T. vaporariorum offspring was found to be highly significantly correlated to parental age on all tomato genotypes except L. hirsutum glabratum. Total reproduction, truncated population counts, and longevity appear good criteria for selection. This test, focusing on antibiotic factors, shows large differences between the resistant and susceptible parent genotypes, but much smaller differences between the breeding lines and the susceptible parent. Earlier screenings relying on a variety of tests appear to have maintained antixenotic rather than antibiotic properties in the breeding lines.     

Parentage analysis of Ansell's mole‐rat family groups indicates a high reproductive skew despite relatively relaxed ecological constraints on dispersal

To better understand evolutionary pathways leading to eusociality, interspecific comparisons are needed, which would use a common axis, such as that of reproductive skew, to array species. African mole‐rats (Bathyergidae, Rodentia) provide an outstanding model of social evolution because of a wide range of social organizations within a single family; however, their reproductive skew is difficult to estimate, due to their cryptic lifestyle. A maximum skew could theoretically be reached in groups where reproduction is monopolized by a stable breeding pair, but the value could be decreased by breeding‐male and breeding‐female turnover, shared reproduction and extra‐group mating. The frequency of such events should be higher in species or populations inhabiting mesic environments with relaxed ecological constraints on dispersal. To test this prediction, we studied patterns of parentage and relatedness within 16 groups of Ansell's mole‐rat (Fukomys anselli) in mesic miombo woodland. Contrary to expectation, there was no shared reproduction (more than one breeder of a particular sex) within the studied groups, and proportion of immigrants and offspring not assigned to current breeding males was low. The within‐group parentage and relatedness patterns observed resemble arid populations of ‘eusocial’ Fukomys damarensis, rather than a mesic population of ‘social’ Cryptomys hottentotus. As a possible explanation, we propose that the extent ecological conditions affect reproductive skew may be markedly affected by life history and natural history traits of the particular species and genera.     

Sexual selection has minimal impact on effective population sizes in species with high rates of random offspring mortality: An empirical demonstration using fitness distributions

The effective population size (N_e) is a fundamental parameter in population genetics that influences the rate of loss of genetic diversity. Sexual selection has the potential to reduce N_e by causing the sex‐specific distributions of individuals that successfully reproduce to diverge. To empirically estimate the effect of sexual selection on N_e, we obtained fitness distributions for males and females from an outbred, laboratory‐adapted population of Drosophila melanogaster. We observed strong sexual selection in this population (the variance in male reproductive success was ～14 times higher than that for females), but found that sexual selection had only a modest effect on N_e, which was 75% of the census size. This occurs because the substantial random offspring mortality in this population diminishes the effects of sexual selection on N_e, a result that necessarily applies to other high fecundity species. The inclusion of this random offspring mortality creates a scaling effect that reduces the variance/mean ratios for male and female reproductive success and causes them to converge. Our results demonstrate that measuring reproductive success without considering offspring mortality can underestimate N_e and overestimate the genetic consequences of sexual selection. Similarly, comparing genetic diversity among different genomic components may fail to detect strong sexual selection.     

Early reproductive investment,senescence and lifetime reproductive success in female Asian elephants

The evolutionary theory of senescence posits that as the probability of extrinsic mortality increases with age, selection should favour early‐life over late‐life reproduction. Studies on natural vertebrate populations show early reproduction may impair later‐life performance, but the consequences for lifetime fitness have rarely been determined, and little is known of whether similar patterns apply to mammals which typically live for several decades. We used a longitudinal dataset on Asian elephants (Elephas maximus) to investigate associations between early‐life reproduction and female age‐specific survival, fecundity and offspring survival to independence, as well as lifetime breeding success (lifetime number of calves produced). Females showed low fecundity following sexual maturity, followed by a rapid increase to a peak at age 19 and a subsequent decline. High early life reproductive output (before the peak of performance) was positively associated with subsequent age‐specific fecundity and offspring survival, but significantly impaired a female's own later‐life survival. Despite the negative effects of early reproduction on late‐life survival, early reproduction is under positive selection through a positive association with lifetime breeding success. Our results suggest a trade‐off between early reproduction and later survival which is maintained by strong selection for high early fecundity, and thus support the prediction from life history theory that high investment in reproductive success in early life is favoured by selection through lifetime fitness despite costs to later‐life survival. That maternal survival in elephants depends on previous reproductive investment also has implications for the success of (semi‐)captive breeding programmes of this endangered species.     

COOPERATIVE BREEDING FAVORS MATERNAL INVESTMENT IN SIZE OVER NUMBER OF EGGS IN SPIDERS

The transition to cooperative breeding may alter maternal investment strategies depending on density of breeders, extent of reproductive skew, and allo‐maternal care. Change in optimal investment from solitary to cooperative breeding can be investigated by comparing social species with nonsocial congeners. We tested two hypotheses in a mainly semelparous system: that social, cooperative breeders, compared to subsocial, solitarily breeding congeners, (1) lay fewer and larger eggs because larger offspring compete better for limited resources and become reproducers; (2) induce egg size variation within clutches as a bet‐hedging strategy to ensure that some offspring become reproducers. Within two spider genera, Anelosimus and Stegodyphus, we compared species from similar habitats and augmented the results with a mini‐meta‐analysis of egg numbers depicted in phylogenies. We found that social species indeed laid fewer, larger eggs than subsocials, while egg size variation was low overall, giving no support for bet‐hedging. We propose that the transition to cooperative breeding selects for producing few, large offspring because reproductive skew and high density of breeders and young create competition for resources and reproduction. Convergent evolution has shaped maternal strategies similarly in phylogenetically distant species and directed cooperatively breeding spiders to invest in quality rather than quantity of offspring.     

Floral density and co-occurring congeners alter patterns of selection in annual plant communities*

Although the evolution and diversification of flowers is often attributed to pollinator-mediated selection, interactions between co-occurring plant species can alter patterns of selection mediated by pollinators and other agents. The extent to which both floral density and congeneric species richness affect patterns of net and pollinator-mediated selection on multiple co-occurring species in a community is unknown and is likely to depend on whether co-occurring plants experience competition or facilitation for reproduction. We conducted an observational study of selection on four species of Clarkia (Onagraceae) and tested for pollinator-mediated selection on two Clarkia species in communities differing in congeneric species richness and local floral density. When selection varied with community context, selection was generally stronger in communities with fewer species, where local conspecific floral density was higher, and where local heterospecific floral density was lower. These patterns suggest that intraspecific competition at high densities and interspecific competition at low densities may affect the evolution of floral traits. However, selection on floral traits was not pollinator mediated in Clarkia cylindrica or Clarkia xantiana, despite variation in pollinator visitation and the extent of pollen limitation across communities for C. cylindrica. As such, interactions between co-occurring species may alter patterns of selection mediated by abiotic agents of selection.