REPRODUCTIVE SKEW AND SPLIT SEX RATIOS IN SOCIAL HYMENOPTERA

Abstract I present a model demonstrating that, in social Hymenoptera, split sex allocation can influence the evolution of reproductive partitioning (skew). In a facultatively polygynous population (with one to several queens per colony), workers vary in their relative relatedness to females (relatedness asymmetry). Split sex‐ratio theory predicts that workers in monogynous (single‐queen) colonies should concentrate on female production, as their relatedness asymmetry is relatively high, whereas workers in the polygynous colonies should concentrate on male production, as their relatedness asymmetry is relatively low. By contrast, queens in all colonies value males more highly per capita than they value females, because the worker‐controlled population sex ratio is too female‐biased from the queens' standpoint. Consider a polygynous colony in a facultatively polygynous population of perennial, social Hymenoptera with split sex ratios. A mutant queen achieving reproductive monopoly would gain from increasing her share of offspring but, because the workers would assess her colony as monogynous, would lose from the workers rearing a greater proportion of less‐valuable females from the colony's brood. This sets an upper limit on skew. Therefore, in social Hymenoptera, skew evolution is potentially affected by queen‐worker conflict over sex allocation.     

INBREEDING DEPRESSION VARIES WITH INVESTMENT IN SEX IN A FACULTATIVE PARTHENOGEN

The reproductive mode of facultative parthenogens allows recessive mutations that accumulate during the asexual phase to be unmasked following sexual reproduction. Longer periods of asexual reproduction should increase the accumulation of deleterious mutations within individuals, reduce population-level genetic diversity via competition and increase the probability of mating among close relatives. Having documented that the investment in sexual reproduction differs among populations and clones of Daphnia pulicaria , we ask if this variation is predictive of the level of inbreeding depression across populations. In four lake populations that vary in sex investment, we raised multiple families (mother, field-produced daughter, laboratory-produced daughter) on high food and estimated the fitness reduction in both sexually produced offspring relative to the maternal genotype. Inbred individuals had lower fitness than their field-produced siblings. The magnitude of fitness reduction in inbred offspring increased as population-level investment in sex decreased. However, there was less of a fitness reduction following sex in the field-produced daughters, suggesting that many field-collected mothers were involved in outcross mating.     

FLORAL SEX ALLOCATION IN SEQUENTIALLY BLOOMING PLANTS

In plants whose flowers develop in a sequence, different flowers may exhibit temporal variation in pollen donation and receipt such that the fitness contributions through male and female functions can vary among flowers. Dichogamy, or directional pollinator movements within inflorescences, can create situations where flowers in different stages in the sequence may differ in the numbers of flowers in the female stage available as potential mates. We present an evolutionarily stable strategy (ESS) analysis of the resource allocations expected in different flowers in hermaphroditic plants when the mating environments vary among flowers. This introduces a modular element into sex-allocation models. Our analysis shows that such variation in the mating environments of flowers can select for differences in sex allocation between flowers. When male and female fertilities are nonlinear functions of the allocations, variation in resource availability can also select for variation in sex allocation among flowers. The influence of dichogamy and pollinator directionality on floral sex allocation is discussed, and the empirical evidence supporting the predictions derived from the model is briefly reviewed. The implications of our results for the evolution of andromonoecy and monoecy are discussed.     

ADAPTIVE SEX ALLOCATION IN A SIMULTANEOUS HERMAPHRODITE

When applied to hermaphrodite organisms, the local mate competition hypothesis predicts an increase of the ratio of sperm to ova produced as the number of mates increases. Here we test this prediction using a hermaphroditic platyhelminth parasite (trematode), Echinostoma caproni. This worm inhabits the small intestine of vertebrates, inevitably inducing the formation of highly subdivided populations, a condition known to promote local mate competition. Moreover this echinostome exhibits an unrestricted mating pattern involving both selfing and outcrossing as well as multiple fertilizations. We quantified the investment in reproductive organs by estimations of testes, cirrus sac, ovary, and egg size and fecundity when echinostomes were isolated alone, in pairs, or in groups of 20 worms. Adult body size was also recorded as a covariate. When mating group size increases (singles, pairs, or groups) we observed a significant increase in resource allocation to male function in addition to a significant decrease in ovary size. Smaller ovaries do not seem to affect egg size, but do result in a reduction in fecundity. Finally, our results are in accordance with the expected theoretical relationship between male allocation and the number of potential mates given local mate competition.     

SEX ALLOCATION IN THE MONOECIOUS HERB BEGONIA SEMIOVATA

Sex-allocation models predict that the evolution of self-fertilization should result in a reduced allocation to male function and pollinator attraction in plants. The evolution of sex allocation may be constrained by both functional and genetic factors, however. We studied sex allocation and genetic variation for floral sex ratio and other reproductive traits in a Costa Rica population of the monoecious, highly selfing annual Begonia semiovata. Data on biomass of floral structures, flower sex ratios, and fruit set in the source population were used to calculate the average proportion of reproductive allocation invested in male function. Genetic variation and genetic correlations for floral sex ratio and for floral traits related to male and female function were estimated from the greenhouse-grown progeny of field-collected maternal families. The proportion of reproductive biomass invested in male function was low (0.34 at flowering, and 0.07 for total reproductive allocation). Significant among-family variation was detected in the size (mass) of individual male and female flowers, in the proportion of male flowers produced, and in the proportion of total flower mass invested in male flowers. Significant among-family variation was also found in flower number per inflorescence, petal length of male and female flowers, and petal number of female flowers. Except for female petal length, we found no difference in the mean value of these characters between selfed and outcrossed progeny, indicating that, with the possible exception of female petal length, the among-family variation detected was not the result of variation among families in the level of inbreeding. Significant positive phenotypic and broad-sense genetic correlations were detected between the mass of individual male and female flowers, between male and female petal length, and between number of male and number of female flowers per inflorescence. The ratio of stamen-to-pistil mass (0.33) was low compared to published data for autogamous species with hermaphroditic flowers, suggesting that highly efficient selfing mechanisms may evolve in monoecious species. Our results indicate that the study population harbors substantial genetic variation for reproductive characters. The positive genetic correlation between investment in male and female flowers may reflect selection for maximum pollination efficiency, because in this self-pollinating species, each female flower requires a neighboring male flower to provide pollen.     

TESTS OF SEX ALLOCATION THEORY IN SIMULTANEOUSLY HERMAPHRODITIC ANIMALS

Sex allocation is a crucial life-history parameter in all sexual organisms. Over the last decades a body of evolutionary theory, sex allocation theory, was developed, which has yielded capital insight into the evolution of optimal sex allocation patterns and adaptive evolution in general. Most empirical work, however, has focused on species with separate sexes. Here I review sex allocation theory for simultaneous hermaphrodites and summarize over 50 empirical studies, which have aimed at evaluating this theory in a diversity of simultaneous hermaphrodites spanning nine animal phyla. These studies have yielded considerable qualitative support for several predictions of sex allocation theory, such as a female-biased sex allocation when the number of mates is limited, and a shift toward a more male-biased sex allocation with increasing numbers of mates. In contrast, many fundamental assumptions, such as the trade-off between male and female allocation, and numerous predictions, such as brooding limiting the returns from female allocation, are still poorly supported. Measuring sex allocation in simultaneously hermaphroditic animals remains experimentally demanding, which renders evaluation of more quantitative predictions a challenging task. I identify the main questions that need to be addressed and point to promising avenues for future research.     

SEX ALLOCATION IN THE ANT COLOBOPSIS NIPPONICUS (WHEELER). I. POPULATION SEX RATIO

The relative power of queens and workers at controlling sex allocation in the ant Colobopsis nipponicus is investigated in this study. Results show that C. nipponicus completely satisfies Hamilton's assumptions concerning colony social structure: monogyny, monoandry, and no worker reproduction. A genetic survey of the population structure rejects possibilities of local mate competition, local resource enhancement, and local resource competition, which all can bias population-allocation ratios from 0.5. Although these factors are absent, the observed sex-allocation ratio (male investment/total sexual investment; 0.250 ± 0.027) is significantly biased toward females and is not different from the estimated optimal ratio for workers (0.252). Thus, it appears that workers are likely to win in conflicts over sex allocation with queens.     

5种毛茛科植物个体大小依赖的繁殖分配和性分配

 植物繁殖分配和性分配是生活史理论的核心问题,一直受到生态学家、进化生物学家们的关注。通过对青藏高原东部高寒草甸(3 500 m)及亚高山草甸(2 900 m)毛茛科5种虫媒两性花植物花期的繁殖分配和性分配的研究发现：1）个体越大,繁殖投入越高,繁殖分配越低,与以往研究结果一致;2）性分配是个体大小依赖的,大个体更偏向雌性器官的资源投入,花粉胚珠比与个体大小的关系较复杂,因种而异;3）花期雌雄功能之间存在资源分配上的权衡（Trade-off）,并且种群之间有差异,表明其受环境条件影响。     

VARIATION IN SEX ALLOCATION AND FLORAL MORPHOLOGY IN IPOMOPSIS AGGREGATA (POLEMONIACEAE)

Intrapopulational variation in biomass allocation to male vs. female function was quantified for the hermaphroditic plant Ipomopsis aggregata in terms applicable to sex allocation models. The proportions of flower biomass put into the corolla and calyx averaged 0.59 and 0.20 and were relatively constant across plants. The proportions in the stamens and pistil averaged 0.13 and 0.08, with considerable variation among plants. Phenotypic gender at the time of flowering ranged from 0.34 to 0.77 female. Pistil dry weight was correlated with stigma exsertion. Stamen weight was correlated with corolla width, which influences male pollination success, and was also correlated with anther position and pollen production. Female reproductive success as estimated by seeds per flower showed no detectable relationship with initial allocation of biomass at the time of flowering, but decreased in accelerating fashion with the proportion of final biomass including seeds that was allocated to male function.     

SEX ALLOCATION ADJUSTMENT TO MATING GROUP SIZE IN A SIMULTANEOUS HERMAPHRODITE

Sex allocation theory is considered as a touchstone of evolutionary biology, providing some of the best supported examples for Darwinian adaptation. In particular, Hamilton's local mate competition theory has been shown to generate precise predictions for extraordinary sex ratios observed in many separate‐sexed organisms. In analogy to local mate competition, Charnov's mating group size model predicts how sex allocation in simultaneous hermaphrodites is affected by the mating group size (i.e., the number of mating partners plus one). Until now, studies have not directly explored the relationship between mating group size and sex allocation, which we here achieve in the simultaneously hermaphroditic flatworm Macrostomum lignano. Using transgenic focal worms with ubiquitous expression of green‐fluorescent protein (GFP), we assessed the number of wild‐type mating partners carrying GFP+ sperm from these focal worms when raised in different social group sizes. This allowed us to test directly how mating group size was related to the sex allocation of focal worms. We find that the proportion of male investment initially increases with increasing mating group size, but then saturates as predicted by theory. To our knowledge, this is the first direct test of the mating group size model in a simultaneously hermaphroditic animal.     

TESTING MODELS OF FACULTATIVE SEX RATIO ADJUSTMENT IN THE POLLINATING FIG WASP PLATYSCAPA AWEKEI

Female hymenoptera are renowned for their ability to adjust offspring sex ratio to local mate competition. When two females share a patch, they frequently produce clutches that differ in size, the female with the larger clutch optimally producing a more female‐biased sex ratio and vice versa. Females can base their sex allocation on their own clutch size only (“self‐knowledge”) or on both females’ clutch sizes (“complete knowledge”). Few studies have genotyped offspring so that each mother's contribution can be considered separately while none has found that both sources of information are used simultaneously. We genotyped 2489 wasps from 28 figs and assigned their maternity to one of the two foundress females. We argue that likelihood is a very convenient method to compare alternative models, while fitness calculations help to appreciate the cost of maladaptation. We find that the pollinating fig wasp Platyscapa awekei simultaneously uses its own as well as the other females clutch size in allocating sex. Indeed, the complete knowledge model explains the data 36 times better than the self‐knowledge model. However, large clutches contained fewer males than the optimal predictions leading to a median selection coefficient of 0.01.     

FEMALE-BIASED SEX RATIOS IN A FACULTATIVELY SOCIAL BEE AND THEIR IMPLICATIONS FOR SOCIAL EVOLUTION

Montane populations of the Australian allodapine bee, Exoneura bicolor, are characterized by high levels of cooperative nesting and strongly female-biased sex ratios. A conspecific population from heathland shows much lower levels of cooperative nesting and lower levels of female bias. In both habitats, sex-ratio bias is greatest in the smallest brood sizes and becomes successively less biased in larger broods. Parity is approached in the largest heathland colonies, but not for any brood-size category in montane areas. Adult intracolony relatedness is moderately high for colonies in both reused and newly founded nests in the montane habitat, but probably low or zero for newly founded nests in heathland. Colony efficiency, measured as the number of brood per adult, increases with colony size in both habitats, suggesting that cooperation between females increases mean female fitness. It is argued that patterns of sex allocation are consistent with nonlinear fitness-return models, in which the mean reproductive value of daughters increases with the number of daughters produced in a brood. Such increases probably arise from a number of social interactions, including cooperative brood defense, increased task efficiency, and lower per capita costs in nest construction. The term “local fitness enhancement” is introduced here to describe these effects collectively. The female-biased ratios should lower selective thresholds for sib-directed altruism, at least in the earlier stages of colony development. It is argued that local fitness enhancement facilitates eusociality in allodapine bees and could also play a role in other haplodiploid taxa, provided cooperative nesting largely involves sisters, colony efficiency increases with colony size, and optimal colony sizes are only achieved after two or more generations after founding.     

植物性别分配与植物群落中物种多样性的维持

植物群落中物种多样性的维持是当代生态学领域中的一个核心问题。根据高斯竞争排除法则,占有相同生态位的物种不能共存。然而植物群落中共存种的数目经常可达数十个以上,难于用以竞争排除法则为基础的竞争共存理论加以解释。本文根据性别分配理论提出了一个新的植物种竞争共存机制;它可以允许占有相同生态位的物种共存。     

QUEEN NUMBER IN COLONIES OF SOCIAL HYMENOPTERA AS A KIN-SELECTED ADAPTATION

Using a series of kin-selection models, I examine factors that favor multiple egg-laying queens (polygyny) in eusocial Hymenoptera colonies. One result is that there is a theoretical conflict of interest between the founding queens and their daughter workers over how many and which individuals should be the extra reproductives. Both castes should prefer their full sisters. Therefore, primary polygyny (multiple related foundresses) may favor queens while secondary polygyny (related queens added to mature colonies) may favor workers. Polygyny, itself, was found to be favored by high colony survivorship and low probability of queens contributing eggs to successive broods. Polygyne colonies, however, did not need to produce more offspring per brood to be selectively favored; they could be half as productive per brood as monogyne ones and still have higher lifetime fitness under some conditions. For reproductive data from eight ant species with both monogyne and polygyne colonies, the model generates results that are consistent with a kin-selection explanation of polygyny in all of them. It is proposed that queen number is an ecologically flexible trait that is influenced by a broad set of factors but is not necessarily linked to specific habitat types. Furthermore, neither polygyny nor monogyny may be reliably considered as the primitive or ancestral Hymenopteran social system. The optimal queen number within a species may evolutionarily increase or decrease, depending on the direction of environmental change.