Coevolution of male and female reproductive traits in a simultaneously hermaphroditic land snail

Inter- and intraspecific studies in gonochoristic animals reveal a covariation between sperm characteristics and the size of the female reproductive tract, indicating a rapid evolutionary divergence, which is consistent with the theory of post-copulatory sexual selection. Simultaneous hermaphrodites differ from species with separate sexes (gonochorists) in that they possess both functional male and female reproductive organs at the same time. We investigated whether in hermaphroditic animals intraspecific variation in reproductive traits results from divergent coevolution, by quantifying the variation in male and female traits among six natural populations of the snail Arianta arbustorum and examining the covariation in interacting traits. There was a significant among-population variation in spermatophore volume, number of sperm transferred and sperm length, as well as in volume of the sperm storage organ (spermatheca) and number of tubules, but not in spermatheca length. We found a positive association between sperm number transferred and spermatheca volume. This result suggests that the same post-copulatory mechanisms as in gonochorists drive the correlated evolution of reproductive characters in hermaphrodites.     

Trade-off between male and female allocation in the simultaneously hermaphroditic flatworm Macrostomum sp

Sex allocation theory for simultaneous hermaphrodites assumes a direct trade-off between the allocation of resources to the male and female reproductive functions. Empirical support for this basic assumption is scarce, possibly because studies rarely control for variation in individual reproductive resource budgets. Such variation, which can have environmental or genetic sources, can generate a positive relationship between male and female investment and can thus obscure the trade-off. In this study on the hermaphroditic flatworm Macrostomum sp. we tried to control for budget effects by restricting food availability in a standardized way and by using an inbred line. We then manipulated mating group size in a two-way design (two group sizes x two enclosure sizes) in order to induce phenotypic variation in male allocation, and expected to find an opposing correlated response in female allocation. The results suggest that we only managed to control the budget effects under some conditions. Under these the sex allocation trade-off emerged. Under the other conditions we found a strongly positive correlation between male and female allocation. We discuss possible causes for the observed differences.     

Masculinization of female golden rabbitfish Siganus guttatus using an aromatase inhibitor treatment during sex differentiation

To elucidate the involvement of endogenous estrogen (estradiol-17beta; E2) and the decisive factor (somatic or germinal element) in the ovarian differentiation of tropical marine teleosts, the effect of the aromatase inhibitor (AI) fadrozole on gonadal sex differentiation in the golden rabbitfish Siganus guttatus (Bloch) was examined for different dosages and periods of treatment. Fadrozole interrupted ovarian cavity formation at a dose of 500 microg g(-1) diet, while there was little effect at 10 or 100 microg g(-1). The gonads from both the 30-day and 90-day administration (500 microg g(-1) diet) groups were significantly biased toward testes (P=0.002 and <0.0001, respectively), which suggests strongly that E2 is involved in early ovarian differentiation and that its suppression is an indispensable condition for testicular differentiation in S. guttatus. The results from the two different AI treatment periods imply that the initial feminization of somatic gonadal elements determines subsequent ovarian differentiation, including oogenesis: a conclusion supported by the considerable time lag between ovarian cavity formation and subsequent oogenesis during normal ovarian differentiation in S. guttatus.     

Structural analysis of female and hermaphroditic flowers of a gynodioecious tree, Ocotea tenera (Lauraceae)

The evolution of gynodioecy from hermaphroditism involves modifications of floral structure such that male or female fitness is enhanced in hermaphrodites and females, respectively. We present an analysis of structural specialization of flowers of Ocotea tenera, in order to evaluate gender system evolution in this tropical tree species. Significant morphological and anatomical variation was found between high fruiting and low or nonfruiting trees. Female flowers were significantly smaller than hermaphroditic flowers, produced no viable pollen, and made relatively greater allocation to structures that increase female fitness. Hermaphroditic flowers were significantly larger than female flowers, produced copious quantities of pollen, and made relatively greater allocation to male structures. Analyses indicated that changes in allometries between whole-flower growth and growth of reproductive structures may have occurred, which enhance function of the flower and plant as a male or female. Efficiency of nutrient allocation for reproduction is argued to be a factor driving gender system evolution in Ocotea tenera.     

A mixed-mating strategy in a hermaphroditic vertebrate

Mixed-mating systems, in which hermaphrodites can either self-fertilize or outcross, are common in many species of plants and invertebrates and have been informative models for studying the selective forces that can maintain both inbreeding and outbreeding in populations. Here, we document a remarkable instance of evolutionary convergence to an analogous mixed mating system by a vertebrate, the mangrove killifish (Kryptolebias marmoratus). In this androdioecious species, most individuals are simultaneous hermaphrodites that characteristically self-fertilize, resulting in local populations that consist of (nearly) homozygous lines. Most demes are also genetically diverse, an observation traditionally attributed to de novo mutation coupled with high levels of inter-site migration. However, data presented here, from a survey of 35 microsatellite loci in Floridian populations, show that genotypic diversity also stems proximally from occasional outcross events that release 'explosions' of transient recombinant variation. The result is a local population genetic pattern (of extensive genotypic variety despite low but highly heterogeneous intra-individual heterozygosities) that differs qualitatively from the genetic architectures known in any other vertebrate species. Advantages of a mixed-mating strategy in K. marmoratus probably relate to this fish's solitary lifestyle and its ability to colonize new habitats.     

Masculinization of the X Chromosome in the Pea Aphid

Evolutionary theory predicts that sexually antagonistic mutations accumulate differentially on the X chromosome and autosomes in species with an XY sex-determination system, with effects (masculinization or feminization of the X) depending on the dominance of mutations. Organisms with alternative modes of inheritance of sex chromosomes offer interesting opportunities for studying sexual conflicts and their resolution, because expectations for the preferred genomic location of sexually antagonistic alleles may differ from standard systems. Aphids display an XX/X0 system and combine an unusual inheritance of the X chromosome with the alternation of sexual and asexual reproduction. In this study, we first investigated theoretically the accumulation of sexually antagonistic mutations on the aphid X chromosome. Our results show that i) the X is always more favourable to the spread of male-beneficial alleles than autosomes, and should thus be enriched in sexually antagonistic alleles beneficial for males, ii) sexually antagonistic mutations beneficial for asexual females accumulate preferentially on autosomes, iii) in contrast to predictions for standard systems, these qualitative results are not affected by the dominance of mutations. Under the assumption that sex-biased gene expression evolves to solve conflicts raised by the spread of sexually antagonistic alleles, one expects that male-biased genes should be enriched on the X while asexual female-biased genes should be enriched on autosomes. Using gene expression data (RNA-Seq) in males, sexual females and asexual females of the pea aphid, we confirm these theoretical predictions. Although other mechanisms than the resolution of sexual antagonism may lead to sex-biased gene expression, we argue that they could hardly explain the observed difference between X and autosomes. On top of reporting a strong masculinization of the aphid X chromosome, our study highlights the relevance of organisms displaying an alternative mode of sex chromosome inheritance to understanding the forces shaping chromosome evolution.     

Size-dependent gender modification in a hermaphroditic perennial herb

The size-advantage model predicts that hermaphroditic organisms adjust sex allocation depending on their resource status. We investigated the relationship between size and sex allocation in the co-sexual perennial herbs Trillium erectum and Trillium grandiflorum at two sites in southern Ontario, Canada by measuring pollen and ovule production and biomass allocation at flowering and fruiting. In both species, there was a strong relationship between size and gender; larger plants allocated proportionately more biomass to female reproduction and produced fewer pollen grains relative to ovules than smaller plants. Variation in gender was better explained by size than age, although age and size were correlated. While the relationship between size and gender was similar between species, T. erectum allocated proportionately more to female reproduction than T. grandiflorum, independent of size. In the absence of pollen limitation, there was no evidence of secondary adjustment of gender at fruiting. The results are discussed in the context of models predicting size-dependent gender modification in animal-pollinated plants. Evidence about the pollination and seed dispersal biology of Trillium spp. suggests that the relative effects of local mate and resource competition may be important in driving size-dependent sex allocation in these species.     

The role of female competition in the mating success of two clones of the Amazon molly, Poecilia formosa

Clones of the unisexual fish Poecilia formosa , the Amazon molly, live in the wild in association with their progenitor bisexual species, and compete with them for resources. These resources include food, space and also mates, since the Amazon molly reproduces gynogenetically, a process in which sperm transferred from a male host species activates their eggs. Earlier studies of the adaptive mechanisms that facilitate the coexistence of the bisexual and unisexual forms have focused upon male behaviour, but recent work with another unisexual species, Poeciliopsis , demonstrated that female aggressive behaviour may play an important part in determining the ecological standing of a clone.
We have extended our observations to female mating behaviour in two clones in the Amazon molly; clone 1 that does not thrive well under laboratory culture; and clone 2 that is hardy and survives very well. There was no aggression between the clones, nor did the clones show aggression towards females of the bisexual species. However, clone 1 consistently was more successful in the number of mating encounters made with the male; it approached the male more often than clone 2 and fled from the male less often. Males also showed some preference for mating with clone 1 females. If there are physiological differences in the wild clones similar to those seen in the laboratory, the mating advantage of the less robust clone 1 may ensure its continued survival in competition with a more vigorous clone.     

Environment-dependent inbreeding depression in a hermaphroditic freshwater snail

Inbreeding depression was simultaneously studied under contrasted environments, laboratory and natural conditions, using individuals originating from 14 families of the freshwater snail Physa acuta. Both survival and growth of juveniles showed inbreeding depression under laboratory conditions. The same fitness components were monitored with mature snails either kept under laboratory conditions or released at a natural site and analysed using capture-mark-recapture models. Genetic composition of both samples was similar. Inbreeding depression on survival was highest in the laboratory while strong outbreeding depression was revealed in the field. Thus inbreeding depression may not be always higher under natural conditions, at the opposite of what is commonly assumed. We suggest that inbreeding depression is dependent on metabolic requirements imposed by the environment. Other evidences showing that inbreeding depression is environment-dependent are reviewed. We conclude that genetic models should include both genetic and environmental variance in inbreeding depression for studying mating system evolution.     

Masculinization and defeminization induced in female hamsters by neonatal treatment with estradiol, RU-2858, and nafoxidine

Newborn female hamsters were treated with 0.1 or 1.0 ng of estradiol benzoate (EB), with 1.0 ng–2.0 μg of the synthetic estrogen RU-2858, or with 0.1 or 0.5 μg of the antiestrogen nafoxidine. When adult the animals were treated with EB and progesterone and tested for the display of lordosis and with testosterone propionate and tested for the display of mounting behavior. The EB doses used failed to alter sexual differentiation. RU-2858 masculinized and defeminized in a dose-dependent manner being most effective when given neonatally as two divided doses. Nafoxidine inhibited lordosis without enhancing mounting behavior. The findings support the hypothesis that estrogens may be involved in the normal sexual differentiation process.     

Isolation of a cancer-associated microchromosome in the sperm-dependent parthenogen Poecilia formosa

In the asexual all-female fish species Poecilia formosa, the Amazon molly, supernumerary chromosomes have frequently been found in both laboratory-reared and wild-caught individuals. While wild-caught individuals with B chromosomes are phenotypically indifferent from conspecifics, individuals carrying B chromosomes from recent introgression events in the laboratory show phenotypic changes. Former analyses showed that the expression of a pigment cell locus is associated with the presence of these B chromosomes. In addition, they contain a so far unidentified locus that confers a higher susceptibility to tumor formation in the presence of pigmentation pattern. Isolation by microdissection and hybridization to metaphase chromosomes revealed that they contain one or several sequences with similarity to a highly repetitive pericentromeric and subtelomeric sequence in A chromosomes. Isolation of one particular sequence by AFLP showed that the B chromosomes contain at least 1 copy of an A-chromosomal region which is highly conserved in the whole genus Poecilia, i.e. more than 5 million years old. We propose it to be a single copy sequence.     

Control of social monogamy through aggression in a hermaphroditic shrimp

Introduction

Sex allocation theory predicts that in small mating groups simultaneous hermaphroditism is the optimal form of gender expression. Under these conditions, male allocation is predicted to be very low and overall per-capita reproductive output maximal. This is particularly true for individuals that live in pairs, but monogamy is highly susceptible to cheating by both partners. However, certain conditions favour social monogamy in hermaphrodites. This study addresses the influence of group size on group stability and moulting cycles in singles, pairs, triplets and quartets of the socially monogamous shrimp Lysmata amboinensis, a protandric simultaneous hermaphrodite.

Results

The effect of group size was very strong: Exactly one individual in each triplet and exactly two individuals in each quartet were killed in aggressive interactions, resulting in group sizes of two individuals. All killed individuals had just moulted. No mortality occurred in single and pair treatments. The number of moults in the surviving shrimp increased significantly after changing from triplets and quartets to pairs.

Conclusion

Social monogamy in L. amboinensis is reinforced by aggressive expulsion of supernumerous individuals. We suggest that the high risk of mortality in triplets and quartets results in suppression of moulting in groups larger than two individuals and that the feeding ecology of L. amboinensis favours social monogamy.     

Sex allocation in hermaphroditic plants

Hermaphroditic plants allocate their reproductive resources to different functions: male, female and pollinator attraction. While earlier sex-allocation models considered only male and female functions, more recent ones can divide reproductive resources into multiple functions. The basic predictions derived from these models are similar. While most models predict sex allocation at the fruit stage (pollen and seeds), some have examined allocation at the flower stage (pollen and ovules). Selfing rate, mode of pollination and competition among offspring of the same parent are some of the factors that can influence sex allocation among populations. Although the empirical evidence lags behind the theoretical development, sex-allocation theory has been quite successful at predicting trends among populations.     

Sexual asymmetry in hermaphroditic plants

Populations of hermaphroditic plants show variation in ovule and pollen production, so that the implicit assumption that hermaphrodite individuals function half as male and half as female is not valid. Such variation in gamete production results in sexual asymmetry, defined as nonconstant ratios of pollen to ovule production among plants of a population. This article reviews (1) some of the considerable amount of recent evidence for sexual asymmetry and non-equal malelfemale sex functioning in hermaphroditic seed plants, and (2) some models of asymmetry and sex functioning, with emphasis on their biological and evolutionary relevance.     

Resource allocation in a simultaneously hermaphroditic slug with phally polymorphism

The theory of resource allocation assumes that a resource not allocated to one function may be reallocated to another. Thus, in hermaphroditic species, an individual that suppresses the use of one sex function may free resources for the other sex function. We determined the relative importance of male copulatory organs in terms of their fraction of the total dry body weight and tested whether in the pulmonate land slug Deroceras laeve (Müller), individuals that lack the male copulatory organs (aphallics) reallocate this resource towards the female structures and/or towards life-history traits. To this end, we raised 13 families under uniparental reproduction and compared growth, length of the juvenile period, number of eggs produced, percentage of hatched eggs and hatching time among a- and euphallics. We also measured the reproductive and sex allocation of all individuals. Six out of 13 families contained no euphallic individuals. In the other seven families, the proportion of euphallic individuals ranged from 0.13 to 0.43. There was an enormous variation in life-history traits and reproductive and sex allocation among individuals, even among individuals of the same family. Allocation to the male function was very low in euphallic slugs (i.e. 1.35% of the total body dry mass and 12.33% of the total reproductive dry mass). Our results did not reveal a reallocation from the lost male function towards the female function, nor towards one of the life-history traits. Finally, we propose a scenario that could explain the maintenance of phally polymorphism in D. laeve.     

Skeletal extension of Acropora formosa at a fringing reef in the Andaman Sea

A growth study of Acropora formosa (Dana) was conducted in situ at a fringing reef in front of Phuket Marine Biological Center, the Andaman Sea, southern Thailand. Monthly extensions of branches tagged with wire were measured in addition to sunshine, rainfall, settlement of sediment, turbidity, salinity, and temperature. The average extension of coral branches was 8 cm in 344 days. Growth was found to be approximately two times faster during the dry northeast monsoon compared with the wet southwest monsoon. Factors which can cause the observed pattern of growth are discussed.Miscellaneous Contributions from PMBC, Thailand, No. 17