Shifts In Sex Allocation Research Articles

Reproductive ecology of the African baobab: Floral features differ among individuals with different fruit production

The long observed disparity in fruit production among individual trees of the iconic African baobab, Adansonia digitata L. presents a potential challenge for the supply of fruit and seeds for food, medicinal and cosmetic purposes. Moreover, this disparity presents an unsolved mystery with ecological as well as economic implications. African baobabs are hermaphrodites where flowers have both male and female reproductive organs within the same flower. Here we evaluate the reproductive features, pollen-pistil interactions, and pollinator-attractant traits from South African baobabs to investigate whether trees with different fruit production levels have different floral features. We show that morphological traits highlight functional sex differences that match with average fruit production data of our sampled trees. Trees that produce more fruit comprised more functionally female flowers, whereas more functionally male flowers were characteristic of trees that did not produce many fruits. This difference may signify a shift in sex allocation in African baobabs, which suggests that baobabs might be functionally, or cryptically, dioecious. Collectively our data suggest that maintaining both tree types within a landscape is paramount for long-term sustainable harvesting of baobab fruit and seeds.

The inherited bacterial symbiont Hamiltonella influences the sex ratio of an insect host.

In many intracellular symbioses, the microbial symbionts provide nutrients advantageous to the host. However, the function of Hamiltonella defensa, a symbiotic bacterium localized in specialized host cells (bacteriocytes) of a whitefly Bemisia tabaci, is uncertain. We eliminate this bacterium from its whitefly host by two alternative methods: heat treatment and antibiotics. The sex ratio of the host progeny and subsequent generations of Hamiltonella-free females was skewed from 1 : 1 (male : female) to an excess of males, often exceeding a ratio of 20 : 1. B. tabaci is haplodiploid, with diploid females derived from fertilized eggs and haploid males from unfertilized eggs. The Hamiltonella status of the insect did not affect copulation frequency or sperm reserve in the spermathecae, indicating that the male-biased sex ratio is unlikely due to the limitation of sperm but likely to be associated with events subsequent to sperm transfer to the female insects, such as failure in fertilization. The host reproductive response to Hamiltonella elimination is consistent with two alternative processes: adaptive shift in sex allocation by females and a constitutive compensatory response of the insect to Hamiltonella-mediated manipulation. Our findings suggest that a bacteriocyte symbiont influences the reproductive output of female progeny in a haplodiploid insect.

One species to another: sympatric Bt transgene gene flow from Brassica napus alters the reproductive strategy of wild relative Brassica juncea under herbivore treatment.

Since pollen flow or seed dispersal can contribute to transgene persistence in the environment, the sympatric presence of transgenic crops with their wild relatives is an ecological concern. In this study, we tested the hypothesis that proximate growth of a herbivore-resistant Bt crop and wild relatives coupled with the presence of herbivores can increase relative frequency of crop-to-wild transgene flow persistence outside of cultivation. We conducted a field experiment using insect enclosures with and without herbivores with cultivated Bt-transgenic Brassica napus (Bt OSR) and wild brown mustard (Brassica juncea) in pure and mixed stands. Low-density diamondback moth (Plutella xylostella) caterpillar infestation treatments were applied and transgene flow and reproductive organs were measured. Bt-transgenic B. napus produced more ovules and pollen than wild mustard, but the pollen to ovule (P/O) ratio in the two species was not significantly different. Low-level herbivory had no effects on fitness parameters of Bt OSR or wild brown mustard or on the transgene flow frequency. All progeny from wild brown mustard containing the Bt transgene came from mixed stands, with a gene flow frequency of 0.66 %. In mixed stands, wild brown mustard produced less pollen and more ovules than in pure stands of brown mustard. This indicates a decreased P/O ratio in a mixed population scenario. Since a lower P/O ratio indicates a shift in sex allocation towards relatively greater female investment and a higher pollen transfer efficiency, the presence of transgenic plants in wild populations may further increase the potential transgene flow by altering reproductive allocation of wild species.

Experimentally evolved and phenotypically plastic responses to enforced monogamy in a hermaphroditic flatworm.

Sexual selection is considered a potent evolutionary force in all sexually reproducing organisms, but direct tests in terms of experimental evolution of sexual traits are still lacking for simultaneously hermaphroditic animals. Here, we tested how evolution under enforced monogamy affected a suite of reproductive traits (including testis area, sex allocation, genital morphology, sperm morphology and mating behaviour) in the outcrossing hermaphroditic flatworm Macrostomum lignano, using an assay that also allowed the assessment of phenotypically plastic responses to group size. The experiment comprised 32 independent selection lines that evolved under either monogamy or polygamy for 20 generations. While we did not observe an evolutionary shift in sex allocation, we detected effects of the selection regime for two male morphological traits. Specifically, worms evolving under enforced monogamy had a distinct shape of the male copulatory organ and produced sperm with shorter appendages. Many traits that did not evolve under enforced monogamy showed phenotypic plasticity in response to group size. Notably, individuals that grew up in larger groups had a more male-biased sex allocation and produced slightly longer sperm than individuals raised in pairs. We conclude that, in this flatworm, enforced monogamy induced moderate evolutionary but substantial phenotypically plastic responses.

Adaptive sex allocation in anticipation of changes in offspring mating opportunities

Sex allocation theory explains why most species produce equal numbers of sons and daughters, and highlights situations that select for deviation from this norm. Past research has, however, heavily focused on situations with discrete generations. When temporally varying generational overlap affects future mate availability, models predict cyclical shifts in sex allocation, but these predictions have not yet been appropriately tested. Here we provide evidence that mosquitofish (Gambusia holbrooki) populations possess a suitable life history: some autumn-born females bred alongside their own offspring, while such overlap was rare or absent for spring-born females and for all males. Our analytic model of sex allocation for these populations produced a perfect rank-order correlation between observed birth sex ratio biases and theoretical predictions, with stronger biases observed as the extent of female generational overlap increased. This is the first robust evidence that sex allocation theory accounts for cases when mating opportunities vary predictably over time.

Size‐dependent sex allocation and sexual selection in Aplysia kurodai, a hermaphrodite with nonreciprocal mating

Abstract. For simultaneous hermaphrodites, a male‐to‐female shift in sex allocation with growth, and weak sexual selection on the male function, is predicted by many theories, although empirical data for both predictions are insufficient for internally fertilizing hermaphrodites with nonreciprocal mating. To address these issues, I studied mating and egg‐laying behavior of the sea hare, Aplysia kurodai (Gastropoda: Opisthobranchia) in the laboratory. Both frequency and duration of egg laying increased with body weight, indicating that fecundity increased with weight. On the other hand, frequency and duration of mating as males did not increase with body weight, suggesting that sperm usage was independent of weight. Therefore, sex allocation shifted from male to female functions with growth. The lack of a relationship between body weight and mating activities as males also suggests that there was no “female” choice for large partners. However, the frequency of mating as females increased with body weight, suggesting “male” choice for large partners. This “male” choice is further supported by the presence of size‐assortative mating and a longer duration of mating when the female partner was large. In addition, the variance in mating frequency as females was larger than that as males. As a whole, the mating behavior in A. kurodai can be summarized as choosy as males and unchoosy as females, the opposite of the patterns known in most gonochoric and hermaphroditic animals.

Sexual dimorphism and the genetic potential for evolution of sex allocation in the gynodioecious plant, Schiedea salicaria

Sex allocation theory addresses how separate sexes can evolve from hermaphroditism but little is known about the genetic potential for shifts in sex allocation in flowering plants. We tested assumptions of this theory using the common currency of biomass and measurements of narrow-sense heritabilities and genetic correlations in Schiedea salicaria, a gynodioecious species under selection for greater differentiation of the sexes. Female (carpel) biomass showed heritable variation in both sexes. Male (stamen) biomass in hermaphrodites also had significant heritability, suggesting the potential for further evolution of dioecy. Significant positive genetic correlations between females and hermaphrodites in carpel mass may slow differentiation between the sexes. Within hermaphrodites, there were no negative genetic correlations between male and female biomass as assumed by models for the evolution of dioecy, suggesting that S. salicaria is capable of further changes in biomass allocation to male and female functions and evolution toward dioecy.

Male mating opportunities affect sex allocation in a protrandric-simultaneous hermaphroditic shrimp

Sex allocation theory predicts phenotypic adjustments by individuals in their investments into the male and female reproductive function in response to environmental conditions. I tested for phenotypically plastic shifts in sex allocation in a protandric simultaneous hermaphrodite, in which individuals mature and reproduce as males first, and later in life, as simultaneous hermaphrodites. I predicted that initially maturing males should adjust the timing of maturation as hermaphrodites according to male mating opportunities mediated by population size of hermaphrodites. In a first experiment, males maintained with only one hermaphrodite reduced the time they spent as males in comparison to males maintained with no conspecifics, presumably because total reproductive output is maximized by two individuals being simultaneous hermaphrodites when the mating system is a pair. Conversely, males maintained in groups with two or more hermaphrodites increased the time they spent as males in comparison to single males. This delay in maturation was not an effect of resource depletion with increasing shrimp density because the growth rate of males did not differ among most of the experimental treatments. One hypothesis to explain this social mediation of sex allocation is that the smaller males are more successful in mating as males than are the larger hermaphrodites: it will pay reproductively for males to delay maturation as hermaphrodites in large but not in small groups. In agreement with this notion, a second experiment demonstrated that smaller males were four times more successful than were larger hermaphrodites in inseminating shrimps reproducing as females. The informative cue that males may use to perceive different group sizes deserves further attention.

How outcrossing hermaphrodites sense the presence of conspecifics and suppress female allocation

One of the greatest remaining problems in the field of sex allocation is the variation across species of the extent to which individuals adjust their offspring sex ratio or sex allocation according to environmental conditions. Particularly in the field of sex allocation, there is a lack of research on the mechanisms and cues involved. We address this problem in the outcrossing simultaneous hermaphroditic polychaete Ophryotrocha diadema, which shifts sex allocation by suppressing the female function in the presence of reproductive competitors or multiple partners. We document that O. diadema hermaphrodites can evaluate group size by means of a species-specific chemical released by mature individuals in water. The perception of such a water-borne signal is sufficient to trigger the observed shift in sex allocation, i.e., a suppression of the female function, irrespective of the frequency of encounters with conspecifics. Under natural conditions, such a pheromone will favor partners' encounters and the adjustment of individual sex allocation according to the numbers of reproductive competitors and/or potential partners.

Adaptive production of fighter males: queens of the ant Cardiocondyla adjust the sex ratio under local mate competition.

Hamilton's concept of local mate competition (LMC) is the standard model to explain female-biased sex ratios in solitary Hymenoptera. In social Hymenoptera, however, LMC has remained controversial, mainly because manipulation of sex allocation by workers in response to relatedness asymmetries is an additional powerful mechanism of female bias. Furthermore, the predominant mating systems in the social insects are thought to make LMC unlikely. Nevertheless, several species exist in which dispersal of males is limited and mating occurs in the nest. Some of these species, such as the ant Cardiocondyla obscurior, have evolved dimorphic males, with one morph being specialized for dispersal and the other for fighting with nest-mate males over access to females. Such life history, combining sociality and alternative reproductive tactics in males, provides a unique opportunity to test the power of LMC as a selective force leading to female-biased sex ratios in social Hymenoptera. We show that, in concordance with LMC predictions, an experimental increase in queen number leads to a shift in sex allocation in favour of non-dispersing males, but does not influence the proportion of disperser males. Furthermore, we can assign this change in sex allocation at the colony level to the queens and rule out worker manipulation.

Facultative sex allocation in snow skink lizards (Niveoscincus microlepidotus).

Mathematical models suggest that reproducing females may benefit by facultatively adjusting their relative investment into sons vs. daughters, in response to population-wide shifts in operational sex ratio (OSR). Our field studies on viviparous alpine skinks (Niveoscincus microlepidotus) document such a case, whereby among- and within-year shifts in OSR were followed by shifts in sex allocation. When adult males were relatively scarce, females produced male-biased litters and larger sons than daughters. The reverse was true when adult males were relatively more common. That is, females that were courted and mated by few males produced mainly sons (and these were larger than daughters), whereas females that were courted and mated by many males produced mainly daughters (and these were larger than sons). Maternal body size and condition also covaried with sex allocation, and the shifting pattern of sexual size dimorphism at birth may reflect these correlated effects rather than a discrete component of an evolved sex-allocation strategy.

INTRASPECIFIC VARIATION IN SEX ALLOCATION IN A SIMULTANEOUS HERMAPHRODITE: THE EFFECT OF INDIVIDUAL SIZE.

Within a population of simultaneous hermaphrodites, individuals may vary in both their current reproductive investment (biomass invested in gonads) and in how they allocate that investment between male and female function. In the chalk bass, Serranus tortugarum, estimates of both reproductive allocation and reproductive success as a male and a female can be made for individuals of different sizes. As individuals increase in size, their investment in gamete production increases, and there is a shift in allocation to a stronger female bias. Spawning frequency as a female in pair spawnings and as a male in both pair spawning and streaking (an alternative mating tactic) does not vary with individual size. As a result, larger individuals should release more sperm or eggs per spawn. Size-assortative pair spawning in this species leads to larger individuals having higher potential returns in total male reproductive success than smaller individuals, which should lead to increases in absolute levels of sperm production in larger individuals when individuals compete for fertilizations through sperm competition. However, smaller individuals contribute a smaller proportion of the sperm released in spawns with multiple spawners and thus are under more intense sperm competition than larger individuals, which should select for increases in male allocation in smaller individuals, all else equal. A local-mate-competition (LMC) model predicts that these factors select for increasing absolute male and female investment with individual size but a relative shift to more female-biased allocation as individual size increases. These predictions are supported by gonadal data. The predictions of average male allocation from the quantitative LMC model were 21.6% and 25.7%, whereas the collections averaged 21.3%. This close agreement of both the mean male allocation and its relative shift with individual size between model and data support the hypothesis that size-specific shifts in sex allocation in this species represent an adaptive response to patterns of mating success and sperm competition.

Sex Allocation in Hermaphroditic Sea Basses

Local mate competition theory has emphasized the importance of sperm competition in determining individual patterns of sex allocation in outcrossing hermaphrodites. In this article I develop a more general model of local mate competition that incorporates fertilization efficiency. I use this model to predict interspecific differences in sex allocation. These predictions are tested by using dry weights of male and female gonadal tissue from six species of hermaphroditic sea basses. In all four paired comparisons, when two of the three factors presumed to determine sex allocation patterns are relatively constant, the shift in sex allocation between species is correctly predicted. Neither levels of sperm competition nor the expected effects of spawning behavior on fertilization efficiency can account for all of the differences in sex allocation, although sperm competition does correctly predict the most differences in sex allocation. Overall, the interspecific differences are predicted by either the level of sperm competition or by factors affecting fertilization efficiency. A broader view of local mate competition that includes aspects of sperm competition and the dynamics of fertilization should ultimately provide more accurate predictions of sex allocation in hermaphroditic organisms.