Evolution Of Dioecy Research Articles

Functional dioecy in Morinda parvifolia (Rubiaceae), a species with stigma-height dimorphism

The evolution of dioecy from heterostyly has been well documented, but detailed studies on this transitional process are rare. Here we report the occurrence of cryptic dioecy in a perennial liana species with stigma-height dimorphism, Morinda parvifolia Bartl. ex DC. (Rubiaceae). Floral morphology, ancillary characters and cross compatibility of long-styled (L-morph) and short-styled (S-morph) were examined. L-morph and S-morph display obvious pistil dimorphisms, with the stigma of S-morph lacking papillae cells. Both floral morphs show similar pollen morphology, although pollen viability is higher in S-morph than in L-morph. S-morph flowers produce viable pollen grains but much reduced stigma and set no fruits, functioning as males; L-morphs, although with viable pollen grains and receptive stigmas, exhibit strong self- and intramorph incompatibility, with self- and intramorph pollen tubes arrested in the stigma lobes and the upper part of style, respectively, resulting in L-morphs functioning only as females. The species thus has physiological androdioecy but functional dioecy. This might be the first case showing the possibility that androdioecy could be a mid-stage in the pathway of dioecy evolving from stigma-height dimorphism.

Spatial seed and pollen games: dispersal, sex allocation, and the evolution of dioecy

The evolutionary forces shaping within- and across-species variation in the investment in male and female sex function are still incompletely understood. Despite earlier suggestions that in plants the evolution or cosexuality vs. dioecy, as well as sex allocation among cosexuals, is affected by seed and pollen dispersal, no formal model has explicitly used dispersal distances to address this problem. Here, we present a game-theory model as well as a simulation study that fills in this gap. Our model predicts that dioecy should evolve if seeds and pollen disperse widely and that sex allocation among cosexuals should be biased towards whichever sex function produces more widely dispersing units. Dispersal limitations stabilize cosexuality by reinforcing competition between spatially clumped dispersal units from the same source, leading to saturating fitness returns that render sexual specialization unprofitable. However, limited pollen dispersal can also increase the risk of selfing, thus potentially selecting for dioecy as an outbreeding mechanism. Finally, we refute a recent claim that cosexuals should always invest equally in both sex functions.

Male sterility, fitness gain curves and the evolution of gender specialization from distyly in Erythroxylum havanense

The evolution of dioecy from a monomorphic hermaphroditic condition requires two mutations, one producing females and one producing males. Conversely, a single mutation sterilizing one sexual function in one morph of distylous species would result in functional dioecy because such a mutation also affects the complementary function in the other morph. In this study, we tested these ideas with Erythroxylum havanense, a distylous species with morph-biased male sterility. Based on sex allocation theory we evaluated whether the invasion of thrum females is favoured over the maintenance of this morph cosexuals. Completely male sterile thrum plants obtained higher fitness returns than hermaphrodites or partial male sterile individuals of the same morph, thus favouring the invasion of female thrum plants. We concluded that because fruit production of pin individuals depends on the pollen produced by thrum plants, the invasion of thrum females would result on the evolution of functional dioecy.

Siring Success and Paternal Effects in Heterodichogamous Acer opalus

Heterodichogamy (a dimorphic breeding system comprising protandrous and protogynous individuals) is a potential starting point in the evolution of dioecy from hermaphroditism. In the genus Acer, previous work suggests that dioecy evolved from heterodichogamy through an initial spread of unisexual males. Here, the question is asked as to whether the different morphs in Acer opalus, a species in which males co-exist with heterodichogamous hermaphrodites, differ in various components of male in fitness. Several components of male fertility were analysed. Pollination rates in the male phase were recorded across one flowering period. Pollen viability was compared among morphs through hand pollinations both with pollen from a single sexual morph and also simulating a situation of pollen competition; in the latter experiment, paternity was assessed with microsatellite markers. It was also determined whether effects of genetic relatedness between pollen donors and recipients could influence the siring success. Finally, paternal effects occurring beyond the fertilization process were tested for by measuring the height reached by seedlings with different sires over three consecutive growing seasons. The males and protandrous morphs had higher pollination rates than the protogynous morph, and the seedlings they sired grew taller. No differences in male fertility were found between males and protandrous individuals. Departures from random mating due to effects of genetic relatedness among sires and pollen recipients were also ruled out. Males and protandrous individuals are probably better sires than protogynous individuals, as shown by the higher pollination rates and the differential growth of the seedlings sired by these morphs. In contrast, the fertility of males was not higher than the male fertility of the protandrous morph. While the appearance of males in sexually specialized heterodichogamous populations is possible, even in the absence of a fitness advantage, it is not clear that males can be maintained at an evolutionary equilibrium with two classes of heterodichogamous hermaphrodites.

Origen, mantenimiento y evolución del ginodioicismo

Uno de los rasgos más característicos de las Angiospermas es la gran diversidad de sistemas reproductivos que presentan. Un ejemplo de ello es el ginodioicismo, caracterizado por la coexistencia de plantas hembra (estériles para la función masculina) y hermafroditas en la misma población. En este trabajo se presentan las principales características de las especies ginodioicas, tales como la gran variación de hembras que existe entre las poblaciones. Se explican las tres formas por las que se puede originar y transmitir la esterilidad masculina y sus consecuencias en la dinámica evolutiva. Asimismo, se presentan y discuten las hipótesis que explicarían la permanencia de las hembras en las poblaciones, ya que al carecer de la función masculina, necesitan producir más o mejores semillas para no estar en desventaja respecto a una hermafrodita. Se analizan las principales rutas evolutivas a partir de una condición hermafrodita y las evidencias actuales que sugieren que el ginodioicismo es la principal vía por la que se podría evolucionar a la dioecia. Finalmente, se hace una reflexión acerca del estado actual de la investigación de los sistemas reproductivos en México, poniendo para ello como ejemplo el estudio del ginodioicismo.

Can Specialized Pathogens Colonize Distantly Related Hosts? Schistosome Evolution as a Case Study

Can Specialized Pathogens Colonize Distantly Related Hosts? Schistosome Evolution as a Case Study

Environmental stress and the evolution of dioecy: Wurmbea dioica (Colchicaceae) in Western Australia

Stressful ecological conditions have been implicated in the evolution of separate sexes in plants. Gender dimorphic species are often found in drier habitats than their sexually monomorphic relatives, and gynodioecious populations appear closer to a dioecious state as resources, particularly water, become limiting. This pattern could result if dry conditions decrease the relative seed fitness of cosexual plants, allowing female plants to become established in monomorphic populations. We studied geographical variation in gender expression and biomass allocation among 12 monomorphic and dimorphic populations of Wurmbea dioica along a latitudinal precipitation gradient in southwestern Australia to provide insight into mechanisms by which aridity might favor transitions between sexual systems. Plants in monomorphic and dimorphic populations exhibited contrasting gender expression and patterns of biomass allocation in areas with different levels of precipitation. Among dimorphic populations, lower precipitation was associated with a higher frequency of female plants, and reduced allocation to female function by hermaphrodites during flowering. In contrast, stress conditions had no effect on female allocation at flowering in monomorphic populations. Across latitudes, unisexuals and cosexuals exhibited consistent differences in above ground traits, with cosexuals having larger leaves, taller stems and larger flowers. Although all plants were smaller under drier conditions, cosexuals decreased above ground allocation to vegetative and reproductive structures with decreasing latitude. In contrast, unisexuals increased allocation to reproduction in drier areas at the expense of below ground size. Aridity was associated with reduced flower size among all gender classes, but not with changes in flower number. These data do not support the hypothesis that resource limitation of female allocation in cosexual populations favors the establishment of gender dimorphism in W. dioica. Alternative hypotheses, involving higher selfing rates and enhanced survival of unisexuals relative to cosexuals under resource-limited conditions, are discussed as possible explanations for the origin of dioecy in W. dioica.

Dioécie cryptique chez Geniostoma borbonica, espèce pionnière endémique de La Réunion

In the general context of conservation of insular habitats, the floral biology, natural fecundity, and breeding system of Geniostoma borbonica (Lam.) Spreng. was studied in natural populations. The species, which was initially assumed to be gynodioecious, presents two kinds of individuals, both with morphological hermaphroditic but functionally unisexual flowers. Some individuals produce pollen grains, but neither ovules nor fruit, whereas other fructiferous individuals have anthers without pollen grains. Geniostoma borbonica is the first species in this genus to be reported as dioecious; its floral morphology illustrates an example of cryptic dioecy. This species combines an apomictic breeding system, assuring a fast installation without reproductive constraints, and a reproductive breeding system assuring maintenance of genetic variability in the population. These two breeding systems allow adaptation to evolution of the habitat during plant succession. This point is discussed in the colonization context of pioneer habitats, where herma- phro ditic species are recognized to be advantageous, as well as in the context of the evolution of dioecy in this genus.Key words: cryptic dioecy, pioneer habitat, oceanic island, Geniostoma.

Effects of Inbreeding in Three Populations of the Dioecious Annual Amaranthus cannabinus (Amaranthaceae)

to be a strong selective force leading to the evolution of dioecy. The purpose of this study was to examine the effects of inbreeding on Amaranthus cannabinus (L.) Sauer (water hemp), a dioecious annual. Inbred and outcrossed lines were established in the greenhouse for three New Jersey populations of water hemp, one salt marsh population and two freshwater marsh populations. After two generations of crosses, inbreeding depression was observed in the percentage of germination, leaf size, and plant height. However, the response to inbreeding varied considerably among and within the three populations. Overall, inbreeding depression was low, suggesting that the avoidance of inbreeding was not a strong selective drive for the evolution of dioecy in A. cannabinus. Another selective factor that more likely contributed to the evolution of dioecy in water hemp is increased reproductive efficiency through sex-specific selection.

Phenotypic and genetic correlations among floral traits in two species of Thalictrum.

The evolution of dioecy in plants is expected to be followed by sex-specific selection, leading to sexual dimorphism. The extent of the response to selection depends on the genetic covariance structure between traits both within and between the sexes. Here I describe an investigation to determine phenotypic and genetic correlations between reproductive traits within cryptically dioecious Thalictrum pubescens and within morphologically dioecious T. dioicum. Females of T. pubescens produce flowers having stamens and pistils, appearing hermaphroditic. Genetic correlations were estimated as family-mean correlations among paternal half-sib families. Positive phenotypic and genetic correlations between parts of the same reproductive organs, as the anther and filament of the stamen, indicate developmental associations between these traits in both species. Negative genetic correlations were detected between pistil number and size of reproductive organs in T. dioicum and showed the same direction, but not significance, in T. pubescens. There was a negative phenotypic correlation between the number of stamens and the number of pistils within female flowers of T. pubescens. Within T. pubescens, there was a positive genetic correlation between the number of stamens in males and the number of pistils in females, indicating that floral evolution in males and females may not be independent in this species.

Sex expression, sex‐specific traits, and the effects of salinity on growth and reproduction of Amaranthus cannabinus (Amaranthaceae), a dioecious annual

Amaranthus cannabinus was studied to investigate some of the ecological factors thought to be involved in the evolution of dioecy and to investigate the effects of salinity on sex expression and sex-specific selection. In the field portion of this study, sex ratios, stability of sex expression, spatial distribution, allocation strategies, and phenologies of the sexes were investigated in New Jersey freshwater and salt marsh populations of water hemp. To examine the effects of salinity on vegetative and reproductive development of males and females, plants were grown in the greenhouse at three salinity levels. Adult sex ratios were found to be 1:1. Temporal deviations from a 1:1 sex ratio varied by population and were due to differences in flowering phenology and mortality between the sexes. No plants were observed to change sex expression, and there was no evidence of spatial segregation of the sexes in the field. In both the field and the greenhouse, females allocated more resources to vegetative tissues and had a longer growing period than males. The results of this study suggest that increased reproductive efficiency through sex-specific growth patterns may have been an important selective factor involved in the evolution of dioecy in A. cannabinus.

From pollen dynamics to adaptive dynamics

AbstractOn plants with many flowers, bumblebees tend to visit more flowers in sequence. This induces pollen transfer between flowers on the same plant (geitonogamy). Consequently, in self‐compatible plants the selfing rate increases with the number of simultaneously open flowers on the plant, and pollen export to other plants in the population can be a decelerating function of the number of flowers. I argue that geitonogamy is important in relation to two phenomena. First, it may explain the low number of seeds per flower and the size‐dependent sex allocation observed in some species. Applying sex allocation theory to the boraginaceous Cynoglossum officinale and Echium vulgare shows that hermaphroditism is stable in both species. The predicted evolutionarily stable values for seeds per flower are close to observed values in the field. The model generally predicts that seeds per flower increase with plant size. This prediction is fine for C. officinale but E. vulgare defies the theory. Second, geitonogamy is important in the evolution of dioecy, as already suggested by Darwin. With abiotic pollination the export of pollen to other plants is likely to be proportional to the number of flowers produced, while it decelerates in animal‐pollinated plants. Dioecy can then evolve gradually in a species with abiotic pollination, provided that inbreeding depression exceeds 50%, geitonogamous selfing increases with the number of flowers and that genetic variation exists. With complete pollen discounting as in the models of geitonogamous pollination by animals, hermaphroditism is always stable. The model explains Darwin’s observation that dioecy is more common in wind‐pollinated species and in species in which individuals are large, reproducing with many flowers.

Fertility of exceptional bisexual individuals in four dioecious plant species

Exceptional, very rare, bisexual (hermaphroditic or monoecious) individuals have been detected in strictly dioecious populations of Rhamnus alaternus, R. palaestinus, Bryonia syriaca and Populus euphratica (a single individual in each species). While ordinary male plants in each species exhibited fully normal pollen, and female individuals set a considerable amount of fruit, the exceptional bisexual plants showed a reduction in male or female fertility, or both. This inability of the rare bisexual individuals to fully invest in the two genders suggests that trade-offs between male and female functions possibly play a major role in the breeding systems of these dioecious species, and probably implicates resource allocation (among other factors) as a selective force in the evolution of dioecy.

Quantitative genetics of floral traits in a gynodioecious wild strawberry Fragaria virginiana: implications for the independent evolution of female and hermaphrodite floral phenotypes

The independent evolution of floral phenotype is an important part of the process of gender specialization during the evolution of dioecy from hermaphroditism. However, we have little information on the genetic variation of floral traits in species with separate genders. Gynodioecious species (co-occurrence of females and hermaphrodites) have a breeding system intermediate between hermaphroditism and complete separation of the sexes (dioecy) and thus can provide insight into the genetic architecture underlying floral phenotype with respect to both primary (stamens and carpels) and secondary (petals) sexual traits. I used a nested breeding design to examine the potential for response to selection on floral traits and to examine whether this response would be similar in the two sex morphs of gynodioecious Fragaria virginiana. There was significant genetic variation underlying all floral traits, although narrow-sense heritabilities (ranging from -0.25 to 0.44) were, in most cases, much lower than broad-sense ones (ranging from 0.28 to 1. 53). Moreover, the sex morphs differed significantly in their heritabilities for shared traits, such as stamen length, and showed a tendency towards differing significantly in others, like carpel number and petal length. In addition, correlations between the sex morphs for these traits (ranging from 0.41 to 0.58) were significantly greater than 0, but less than 1. These results indicate that greater sexual dimorphism could evolve in this population of F. virginiana, even if selection on these traits is not divergent. However, strong developmental integration of floral traits (e.g. stamen length and petal length) and high levels of nonadditive genetic variance may represent barriers to the evolution of complete sexual dimorphism.

Persistence of a fig wasp population and evolution of dioecy in figs: a simulation study

AbstractThe relationship between fig trees and their pollinator wasps is a well‐known example of species‐specific obligate mutualism. In this article we present a stochastic model of this mutualistic system, referring to data on a dioecious fig (Ficus schwarzii) in Borneo, and examine the conditions for the persistence of a wasp population for a given period. (1) When the average duration of the flowering interval of fig trees is short, even a small fig population can sustain a wasp population successfully. A population whose average period of flowering cycle is half that of another population can sustain a wasp population with a number of trees less than half of the other population. (2) The wasp survival rate (WSR) is higher when (a) the variation of the interval periods of fig flowering is smaller, (b) the fig population size is larger, and (c) figs can prolong their receptivity to wait for a wasp if no wasps are available. (3) WSR is predictable from the average proportion of the fig's receptive phases, in which wasps are available, to their total receptive phases. (4) The persistence period of a wasp population increases exponentially with the number of fig trees. Based on these results we propose a new hypothesis, as a possible scenario, on the evolution of dioecy from monoecy in Ficus.

Pollination system and evolution of dioecy from distyly in Mussaenda parviflora (Rubiaceae)

AbstractThe floral morphology and reproductive ecology of a scandent shrub species, Mussaenda parviflora Miq. (Rubiaceae), were studied on Iriomote and Amami Ohshima Islands, Japan. The morphological study demonstrated that M. parviflora was gynodioecious. Crossing experiments, however, revealed that it was functionally dioecious. The flowers were visited mainly by butterflies in the daytime and mainly by crepuscular hawkmoths in the evening. Dioecy in this species is thought to have evolved from distyly. Dioecy of this species, which is pollinated by long‐tongued Lepidoptera, is unusual as the evolution of dioecy from distyly in plants with long corolla tubes is thought to have been triggered by a pollinator shift from long‐ to short‐tongued insects. In this species, however, two floral morphological features may have caused the evolution. The first feature is the presence of many upward‐facing hairs covering the inner surface of the upper part of the corolla tube; these hairs appear to have impeded pollen flow from long‐ to short‐styled flowers. The second feature is the overlap in anther height between the two types of flowers, which may have reduced seed set by clogging stigma with incompatible pollen grains. Accordingly, male sterility in long‐styled plants may have evolved.

Reproductive allocation and the long‐term costs of reproduction in Siparuna grandiflora, a dioecious neo‐tropical shrub

1 Using a combination of observational and experimental approaches, both allocation of resources to reproduction (often called the direct cost of reproduction) and the subsequent long‐term costs (the indirect, delayed or demographic cost) associated with reproductive allocation to male and female function in Siparuna grandiflora (Siparunaceae), a tropical dioecious shrub, were examined. 2 The objectives were to determine whether females allocate more biomass or nitrogen per reproductive episode than males, and whether there is a long‐term cost of reproduction in terms of subsequent growth or reproduction for either sex. If there is no long‐term cost of reproduction, then reproduction may be viewed as free in an evolutionary sense. 3 As is generally the case in dioecious species, females allocated more biomass and nitrogen to reproduction than males. Females also showed delayed costs of reproduction in terms of decreased growth and subsequent reproduction, whereas males did not. 4 The lack of measurable delayed costs in males suggests that with the evolution of dioecy, selection has reduced delayed costs of reproduction in S. grandiflora males. In contrast, females that were prevented from reproducing were able to re‐allocate resources to growth, and produced more stem length on average than males. This re‐allocation response may have evolved to reduce delayed costs of reproduction in females over time frames longer than that considered in the present study.

Reproductive trait variation in the functionally dioecious and morphologically heterostylous island endemic Chassalia corallioides (Rubiaceae)

Documenting the floral biology and breeding system of species throughout the Rubiaceae family provides data on the number of times heterostyly and dioecy may have evolved in this large family. The objectives of this paper are to quantify (a) whether Chassalia corallioides, a small tree endemic to La Reunion Island in the Indian Ocean, is another example of the evolution of dioecy from distyly and (b) whether reproductive traits linked to male and female function vary over the ecological distribution of this species. Quantification of pollen production and fruit set following controlled and natural pollinations demonstrate that this species is dioecious. Male flowers have longer corolla tubes than female flowers. Female flowers have long styles with stigmas placed above the anthers whereas males have short styles with stigmas placed below the anthers. Stigmas and anthers are reciprocally placed in each morph, illustrating that the species is morphologically heterostylous. Both fecundity and flower size are negatively correlated with altitude. In male plants, corollas are shorter and wider and anthers are placed closer to the mouth of the corolla tube with increasing altitude. Male plants flowered more often than female plants, the likely cause of the male biased sex ratio in each of the two years studied. The evolution of dioecy in relation to the island biogeography of the region and the diversification of the genus Chassalia is discussed.

Molecular Evolution and Adaptive Radiation.

Preface List of Contributors Part I. Introduction: 1. Adaptive radiation and molecular evolution: concepts and research issues Thomas J. Givnish 2. Homoplasy in molecular vs. morphological data: the likelihood of correct phylogenetic inference Thomas J. Givnish, and Kenneth J. Sytsma Part II. Integrative Studies: 3. Adaptive radiation of the Hawaiian silversword alliance: congruence and conflict of phylogenetic evidence from molecular and non-molecular investigations Bruce G. Baldwin 4. The chronicle of marsupial evolution Mark S. Springer, John A. W. Kirsch, and Judd A. Chase 5. Evolutionary origins of phenotypic diversity in Daphnia John K. Colbourne, Paul D. N. Hebert, and Derek J. Taylor 6. Evolutionary trends in the ecology of New World monkeys inferred from a combined phylogenetic analysis of nuclear, mitochondrial, and morphological data Ines Horovitz, and Axel Meye 7. Adaptive radiation in the aquatic plant family Pontederiaceae: insights from phylogenetic analysis Spencer C. H. Barrett, and Sean W. Graham 8. Molecular evolution and adaptive radiation in Brocchinia (Bromeliaceae: Pitcairnioideae) atop tepuis of the Guayana Shield Thomas J. Givnish, Kenneth J. Sytsma, James F. Smith, William J. Hahn, David H. Benzing, and Elizabeth M. Burkhardt Part III. Convergence: 9. You aren't always what you eat: evolution of nectar-feeding among Old World fruitbats (Megachiroptera: Pteropodidae) John A. W. Kirsch, and Francois-Joseph Lapointe 10. Chloroplast DNA restriction sites and floral versus non-floral characters in the obligate twig epiphytes in subtribe Oncidiinae (Orchidaceae) Mark W. Chase, and Jeffrey D. Palmer 11. Adaptation, cladogenesis, and the evolution of habitat association in North American tiger beetles: a phylogenetic perspective Alfried P. Vogler Part IV. Rapid Radiations: 12. Molecular phylogenetic tests of sympatric speciation models in Lake Malawi cichlid fishes Peter N. Reinthal, and Axel Mey 13. A rapid adaptive radiation due to a key innovation in Aquilegia Scott Hodges 14. Origin and evolution of Argyranthemum (Asteraceae: Anthemideae) in Macaronesia Javier Francisco-Ortega, Daniel J. Crawford, Arnoldo Santos-Guerra, and Robert K. Jansen Part V. Reproductive Strategies: 15. Floral diversification, pollination biology, and molecular evolution in Platanthera (Orchidaceae) Jeffrey R. Hapeman, and Kenneth Inoue 16. Phylogenetic perspectives on the evolution of dioecy: adaptive radiation in the endemic Hawaiian genera Schiedea and Alsinodendron (Caryophyllaceae: Alsinoideae) Ann K. Sakai, Stephen G. Weller, Warren L. Wagner, and Pamela S. Soltis 17. Ecological and reproductive shifts in the diversification of the endemic Hawaiian Drosophila Michael P. Kambysellis, and Elysse M. Craddock Part VI. Character Divergence and Community Assembly: 18. History of ecological selection in sticklebacks - uniting experimental and phylogenetic approaches Eric B. Taylor, James D. McPhail, and Dalph Schluter 19. Phylogenetic studies of convergent adaptive radiations in Caribbean Anolis lizards Todd Jackman, Jonathan B. Losos, Allan Larson, and Kevin de Queiros Part VII. Macroevolutionary Patterns: 20. Molecular and morphological evolution during the post-Palaeozoic diversification of echinoids Andrew B. Smith, and D. T. J. Littlewood 21. How fast is speciation: molecular, geological and phylogenetic evidences from adaptive radiations of fish Amy R. McCune Index.

Pollen morphology and functional dioecy inSolanum (Solanaceae)

Dioecy has evolved independently several times in the large, mostly tropical genusSolanum. In all cases of dioecy inSolanum functionally male flowers have normal anthers, normal pollen and reduced stigmas while functionally female flowers have stigmas and anthers that appear normal but contain non-functional, usually inaperturate pollen. The inaperturate pollen has living cytoplasm, but apparently never germinates and it has been hypothesised that the pollen in these functionally female flowers is retained as a pollinator reward. Pollen morphology is compared in twelve of the thirteen known dioecious species ofSolanum, and some stages in the the development of inaperturate pollen in the anthers of functionally female flowers ofSolanum confertiseriatum of Western Ecuador are examined. Observations on the development and morphology of inaperturate pollen in functionally female flowers ofSolanum are related to hypotheses about the evolution of dioecy in the genus.