Mitochondrial DNA distributions indicate colony propagation by single matri-lineages in the social spider Stegodyphus dumicola (Eresidae)

Colony-dwelling social spiders of the genus Stegodyphus are characterized by high colony turnover, within-colony mating, inbreeding and skewed sex ratios. These phenomena may purge genetic variation from the entire species gene pool. Social Stegodyphus have previously been discussed as ecologically unstable and evolutionary dead ends. We investigated the distribution and age (sequence divergence) of mitochondrial DNA variation for inferences of colony propagation, colony discreteness and maintenance of genetic variation in the social spider S. dumicola . In contrast to our expectations, we found abundant mtDNA variation, consisting of 15 haplotypes belonging to four haplotype lineages. Lineage divergence ranged between 2.75 and 6% for the gene ND1. Nearly all colonies (86%) were monomorphic and even neighbour colonies showed fixed differences. Simulations show that genetic drift in multifounder colonies cannot alone explain monomorphism within colonies. Haplotypes in polymorphic colonies and from neighbouring colonies were always genealogically similar. Monomorphism and the genealogical pattern among colonies suggest 'clonal' colony propagation involving single matrilineages. The divergence of haplotype lineages and distribution of haplotypes imply that colony turnover is not high enough to purge genetic variation in the species gene pool, and that S. dumicola as a species is old enough to question the instability (in ecological time) of a social spider.  © 2002 The Linnean Society of London, Biological Journal of the Linnean Society , 2002, 76 , 591–600.     

Species cohesion despite extreme inbreeding in a social spider

Colonial social spiders experience extreme inbreeding and highly restricted gene flow between colonies; processes that question the genetic cohesion of geographically separated populations and which could imply multiple origins from predecessors with limited gene flow. We analysed species cohesion and the potential for long-distance dispersal in the social spider Stegodyphus dumicola by studying colony structure in eastern South Africa and the cohesion between this population and Namibian populations previously published. Data from both areas were (re)analysed for historic demographic parameters. Eastern South African S. dumicola were closely related to an east Namibian lineage, showing cohesion of S. dumicola relative to its sister species. Colony structure was similar in both areas with mostly monomorphic colonies, but haplotype diversity was much reduced in eastern South Africa. Here, the population structure indicated recent population expansion. By contrast, Namibia constitutes an old population, possibly the geographic origin of the species. Both the comparison of the eastern South African and Namibian lineages and the distribution within eastern South Africa show the potential for long-distance dispersal in few generations via colony propagation.     

The age and evolution of sociality in Stegodyphus spiders: a molecular phylogenetic perspective

Social, cooperative breeding behaviour is rare in spiders and generally characterized by inbreeding, skewed sex ratios and high rates of colony turnover, processes that when combined may reduce genetic variation and lower individual fitness quickly. On these grounds, social spider species have been suggested to be unstable in evolutionary time, and hence sociality a rare phenomenon in spiders. Based on a partial molecular phylogeny of the genus Stegodyphus, we address the hypothesis that social spiders in this genus are evolutionary transient. We estimate the age of the three social species, test whether they represent an ancestral or derived state and assess diversification relative to subsocial congeners. Intraspecific sequence divergence was high in all of the social species, lending no support for the idea that they are young, transient species. The age of the social lineages, constant lineage branching and the likelihood that social species are independently derived suggest that either the social species are 'caught in sociality' or they have evolved into cryptic species.     

Population stability and extinction in a social spider Stegodyphus mimosarum (Araneae: Eresidae)

Nests of social spiders in their natural habitat are clustered and colony clusters may be short-lived. Rapid growth and subsequent extinction of colonies and colony clusters are predicted for social spider populations; however, little quantitative data exist on the longevity of colonies. Furthermore, processes that influence the growth and decline of social spider populations are poorly understood. In this study we followed a population of over 550 nests of S. mimosarum from September 1994 to December 1999 and analysed the changes in relation to abiotic (temperature and rainfall) and biotic (parasitism) factors. We observed two years of apparent population stability (1994–1995), during which nest numbers remained high and constant. This was followed in 1996 by a c. 12% decrease in the numbers of active nests. At the end of 1996 there was a mass dispersal event which was followed in 1997 by a steady decline of the population with no further recovery. Thus, the decline was preceded by dispersal and nest failure, indicating that conditions in the population were unfavourable. The population-wide synchrony of these events reflects the seasonally synchronized development in & mimosarum. However, extrinsic factors related to climate did not explain the extreme events of dispersal and population decline. The potential importance of parasitism, on the one hand, and unknown intrinsic factors on the other, should be considered as alternative explanations that remain to be tested.     

Survival benefits select for group living in a social spider despite reproductive costs

The evolution of cooperation requires benefits of group living to exceed costs. Hence, some components of fitness are expected to increase with increasing group size, whereas others may decrease because of competition among group members. The social spiders provide an excellent system to investigate the costs and benefits of group living: they occur in groups of various sizes and individuals are relatively short-lived, therefore life history traits and Lifetime Reproductive Success (LRS) can be estimated as a function of group size. Sociality in spiders has originated repeatedly in phylogenetically distant families and appears to be accompanied by a transition to a system of continuous intra-colony mating and extreme inbreeding. The benefits of group living in such systems should therefore be substantial. We investigated the effect of group size on fitness components of reproduction and survival in the social spider Stegodyphus dumicola in two populations in Namibia. In both populations, the major benefit of group living was improved survival of colonies and late-instar juveniles with increasing colony size. By contrast, female fecundity, female body size and early juvenile survival decreased with increasing group size. Mean individual fitness, estimated as LRS and calculated from five components of reproduction and survival, was maximized for intermediate- to large-sized colonies. Group living in these spiders thus entails a net reproductive cost, presumably because of an increase in intra-colony competition with group size. This cost is traded off against survival benefits at the colony level, which appear to be the major factor favouring group living. In the field, many colonies occur at smaller size than expected from the fitness curve, suggesting ecological or life history constraints on colony persistence which results in a transient population of relatively small colonies.     

Maternal care and subsocial behaviour in spiders

While most spiders are solitary and opportunistically cannibalistic, a variety of social organisations has evolved in a minority of spider species. One form of social organisation is subsociality, in which siblings remain together with their parent for some period of time but disperse prior to independent reproduction. We review the literature on subsocial and maternal behaviour in spiders to highlight areas in which subsocial spiders have informed our understanding of social evolution and to identify promising areas of future research. We show that subsocial behaviour has evolved independently at least 18 times in spiders, across a wide phylogenetic distribution. Subsocial behaviour is diverse in terms of the form of care provided by the mother, the duration of care and sibling association, the degree of interaction and cooperation among siblings, and the use of vibratory and chemical communication. Subsocial spiders are useful model organisms to study various topics in ecology, such as kin recognition and the evolution of cheating and its impact on societies. Further, why social behaviour evolved in some lineages and not others is currently a topic of debate in behavioural ecology, and we argue that spiders offer an opportunity to untangle the ecological causes of parental care, which forms the basis of many other animal societies.     

The ecological benefits of larger colony size may promote polygyny in ants

How polygyny evolved in social insect societies is a long‐standing question. This phenomenon, which is functionally similar to communal breeding in vertebrates, occurs when several queens come together in the same nest to lay eggs that are raised by workers. As a consequence, polygyny drastically reduces genetic relatedness among nestmates. It has been suggested that the short‐term benefits procured by group living may outweigh the costs of sharing the same nesting site and thus contribute to organisms rearing unrelated individuals. However, tests of this hypothesis are still limited. To examine the evolutionary emergence of polygyny, we reviewed the literature to build a data set containing life‐history traits for 149 Palearctic ant species and combined this data set with a reconstructed phylogeny. We show that monogyny is the ancestral state and that polygyny has evolved secondarily and independently throughout the phylogenetic tree. The occurrence of polygyny is significantly correlated with larger colony size, dependent colony founding and ecological dominance. Although polydomy (when a colony simultaneously uses several connected nests) tends to occur more frequently in polygynous species, this trend is not significant when phylogenetic history is accounted for. Overall, our results indicate that polygyny may have evolved in ants in spite of the reduction in nestmate relatedness because large colony size provides immediate ecological advantages, such as the more efficient use of temporal food resources. We suggest that the competitive context of ant communities may have provided the conditions necessary for the evolution of polygyny in some clades.     

Third Presentation of the Niko Tinbergen-Förderpreis

Cooperative social life originated independently at least 3 times in the eresid spider genus Stegodyphus. The ultimate and proximate factors for sociogenesis have been analyzed in two African social species, S. dumicola and S. mimosarum.

• 1 More profitable hunting as the ultimate benefit of sociality can explain group sizes up to 30 individuals. Most groups are much larger, reducing average female fecundity. They benefit mainly from the shelter against predators provided by the compact silk nest as a heritable resource.
• 2 Sociogenesis is not based on extended maternal care but on interattraction and tolerance of juvenile spiders, retained throughout life in females. Their neotenic sociality came to overlap with advanced (pedomorphic) sexual maturity. This evolutionary pathway towards sociality is called the “sibling-route”.
• 3 Negative side effects, accumulating with group size, may make sociality in Stegodyphus evolutionarily unstable.

     

Sociality in theridiid spiders: repeated origins of an evolutionary dead end

Evolutionary "dead ends" result from traits that are selectively advantageous in the short term but ultimately result in lowered diversification rates of lineages. In spiders, 23 species scattered across eight families share a social system in which individuals live in colonies and cooperate in nest maintenance, prey capture, and brood care. Most of these species are inbred and have highly female-biased sex ratios. Here we show that in Theridiidae this social system originated eight to nine times independently among 11 to 12 species for a remarkable 18 to 19 origins across spiders. In Theridiidae, the origins cluster significantly in one clade marked by a possible preadaptation: extended maternal care. In most derivations, sociality is limited to isolated species: social species are sister to social species only thrice. To examine whether sociality in spiders represents an evolutionary dead end, we develop a test that compares the observed phylogenetic isolation of social species to the simulated evolution of social and non-social clades under equal diversification rates, and find that sociality in Theridiidae is significantly isolated. Because social clades are not in general smaller than their nonsocial sister clades, the "spindly" phylogenetic pattern-many tiny replicate social clades-may be explained by extinction rapid enough that a nonsocial sister group does not have time to diversify while the social lineage remains extant. In this case, this repeated origin and extinction of sociality suggests a conflict between the short-term benefits and long-term costs of inbred sociality. Although benefits of group living may initially outweigh costs of inbreeding (hence the replicate origins), in the long run the subdivision of the populations in relatively small and highly inbred colony lineages may result in higher extinction, thus an evolutionary dead end.     

Spider dragline silk: correlated and mosaic evolution in high-performance biological materials

The evolution of biological materials is a critical, yet poorly understood, component in the generation of biodiversity. For example, the diversification of spiders is correlated with evolutionary changes in the way they use silk, and the material properties of these fibers, such as strength, toughness, extensibility, and stiffness, have profound effects on ecological function. Here, we examine the evolution of the material properties of dragline silk across a phylogenetically diverse sample of species in the Araneomorphae (true spiders). The silks we studied are generally stronger than other biological materials and tougher than most biological or man-made fibers, but their material properties are highly variable; for example, strength and toughness vary more than fourfold among the 21 species we investigated. Furthermore, associations between different properties are complex. Some traits, such as strength and extensibility, seem to evolve independently and show no evidence of correlation or trade-off across species, even though trade-offs between these properties are observed within species. Material properties retain different levels of phylogenetic signal, suggesting that traits such as extensibility and toughness may be subject to different types or intensities of selection in several spider lineages. The picture that emerges is complex, with a mosaic pattern of trait evolution producing a diverse set of materials across spider species. These results show that the properties of biological materials are the target of selection, and that these changes can produce evolutionarily and ecologically important diversity.     

Life-history variation in closely related generalist predators living in the same habitat: a case study with three Cyclosa spiders

1. Generalist predators sharing similar food resources and phenologies as well as having no competitive interactions are expected to have a similar life-history pattern, but some closely related web spiders show different life-history traits. The present paper clarifies possible selection pressures affecting life-history traits of the three coexisting Cyclosa spiders and explores the significance of the life-history variation.
2. Cyclosa argenteoalba had lower daily survival rate and higher growth rate, C. sedeculata had higher daily survival rate and lower growth rate, and C. octotuberculata showed intermediate levels. This implies that the selection pressures these spiders experience differ appreciably even in the same habitat.
3. The significance of the life-history characteristics of the three species was evaluated by general life-history theories. Cyclosa argenteoalba showed distinguishing reproductive traits: shorter time to maturation, larger reproductive effort, larger relative clutch size, decreased clutch size with the number of clutches, and smaller egg size. These characteristics may have evolved in response to the larger ratio of juvenile to adult survivorship. Cyclosa octotuberculata had a clutch size much larger than the other two species, but relative clutch sizes accounting for body size were similar between C. octotuberculata and C. sedeculata . Also, the two species showed a similar time to maturation despite having different selection pressures. Probably, higher growth rate compensates for lower survivorship, leading to the similarity in some reproductive traits.     

Morphological evolution of spiders predicted by pendulum mechanics

Background

Animals have been hypothesized to benefit from pendulum mechanics during suspensory locomotion, in which the potential energy of gravity is converted into kinetic energy according to the energy-conservation principle. However, no convincing evidence has been found so far. Demonstrating that morphological evolution follows pendulum mechanics is important from a biomechanical point of view because during suspensory locomotion some morphological traits could be decoupled from gravity, thus allowing independent adaptive morphological evolution of these two traits when compared to animals that move standing on their legs; i.e., as inverted pendulums. If the evolution of body shape matches simple pendulum mechanics, animals that move suspending their bodies should evolve relatively longer legs which must confer high moving capabilities.

Methodology/Principal Findings

We tested this hypothesis in spiders, a group of diverse terrestrial generalist predators in which suspensory locomotion has been lost and gained a few times independently during their evolutionary history. In spiders that hang upside-down from their webs, their legs have evolved disproportionately longer relative to their body sizes when compared to spiders that move standing on their legs. In addition, we show how disproportionately longer legs allow spiders to run faster during suspensory locomotion and how these same spiders run at a slower speed on the ground (i.e., as inverted pendulums). Finally, when suspensory spiders are induced to run on the ground, there is a clear trend in which larger suspensory spiders tend to run much more slowly than similar-size spiders that normally move as inverted pendulums (i.e., wandering spiders).

Conclusions/Significance

Several lines of evidence support the hypothesis that spiders have evolved according to the predictions of pendulum mechanics. These findings have potentially important ecological and evolutionary implications since they could partially explain the occurrence of foraging plasticity and dispersal constraints as well as the evolution of sexual size dimorphism and sociality.     

Amplified fragment length polymorphism fingerprints support limited gene flow among social spider populations

We used DNA fingerprints to determine whether the population structure and colony composition of the cooperative social spider Stegodyphus dumicola are compatible with requirements of interdemic ('group') selection: differential proliferation of demes or groups and limited gene flow among groups. To investigate gene flow among groups, spiders were collected from nests at 21 collection sites in Namibia. Analysis of molecular variance showed a small but highly significant differentiation among geographic regions (Φ_PT = 0.23, P  = 0.001). Thirty-three nests at four collection sites (6–10 spiders per nest, 292 individual spiders) were investigated in more detail to evaluate variation within and among colonies and among collection sites. In these 33 nests, an average of 15% of loci (fingerprint bands) were polymorphic among nestmates; 16% of observed variance was partitioned among collection sites, 48% among nests within a collection site, and 36% among individuals within nests. Spatial autocorrelation analyses of spiders at three collection sites showed that the maximum extent of detectable spatial autocorrelation among individuals was approximately 30 m, indicating dispersal over greater distances is not typical. These results indicate limited gene flow among nests, as well as spatial structuring at the level of regions, local populations, and nests, compatible with interdemic selection.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 97 , 235–246.     

The functions of societies and the evolution of group living: spider societies as a test case

Many models have been advanced to suggest how different expressions of sociality have evolved and are maintained. However these models ignore the function of groups for the particular species in question. Here we present a new perspective on sociality where the function of the group takes a central role. We argue that sociality may have primarily a reproductive, protective, or foraging function, depending on whether it enhances the reproductive, protective or foraging aspect of the animal's life (sociality may serve a mixture of these functions). Different functions can potentially cause the development of the same social behaviour. By identifying which function influences a particular social behaviour we can determine how that social behaviour will change with changing conditions, and which models are most pertinent. To test our approach we examined spider sociality, which has often been seen as the poor cousin to insect sociality. By using our approach we found that the group characteristics of eusocial insects is largely governed by the reproductive function of their groups, while the group characteristics of social spiders is largely governed by the foraging function of the group. This means that models relevant to insects may not be relevant to spiders. It also explains why eusocial insects have developed a strict caste system while spider societies are more egalitarian. We also used our approach to explain the differences between different types of spider groups. For example, differences in the characteristics of colonial and kleptoparasitic groups can be explained by differences in foraging methods, while differences between colonial and cooperative spiders can be explained by the role of the reproductive function in the formation of cooperative spider groups. Although the interactions within cooperative spider colonies are largely those of a foraging society, demographic traits and colony dynamics are strongly influenced by the reproductive function. We argue that functional explanations help to understand the social structure of spider groups and therefore the evolutionary potential for speciation in social spiders.     

More data, fewer shifts: molecular insights into the evolution of the spinning apparatus in non-orb-weaving spiders

All spiders produce silk and use it for various functions throughout their lives, but not all spiders produce the same silks, or use them for the same functions. These functions may include building shelters, protecting eggs, and trapping prey. The "RTA clade" of spiders (grass spiders, jumping-spiders, wolf spiders, hackled-band weavers, etc.) is an extremely diverse group ( approximately 18,000 species, representing nearly half of all described species), with great variation in ecology and morphology, including variation in the cribellum, a specialized silk-producing organ. The loss of the cribellum, a structure that produces fibers contributing stickiness to prey snares and which is invariably associated with a set of accessory structures, has been studied in orb-web-weavers and shown to have been lost once during the evolutionary history of the group, but never regained. Relative to the orb-weavers, evolution of the structure remains less-thoroughly studied in the RTA clade. As the cribellum is one member of a suite of traits, the combined action of which is essential in prey-capture, its loss should have ecological correlates or physiological trade-offs of evolutionary interest. Using molecular data from nuclear genes (ribosomal DNAs 18S and 28S, and protein-coding Histone H3), as well as mitochondrial data (Cytochrome oxidase I) totaling approximately 3400 base pairs, we developed a phylogenetic hypothesis for three-clawed lineages in this group, focusing on families where taxonomy and previous cladistic analyses suggest multiple losses, or possibly loss and secondary gain, of the cribellum. Results of Bayesian and direct-optimization (POY) analyses agree on a well-resolved and robust agelenid clade that includes the putative subfamilies Ageleninae, Tegenariinae, Textricinae and Coelotinae, but excludes the cribellate New Zealand genus Neoramia. Optimizing the pattern of cribellum evolution onto these trees shows that the cribellate state is conserved in large clades and has undergone fewer shifts than current taxonomy implies. The dominant pattern is one of repeated loss of the cribellum, though loss and regain remains a possibility in some groups.     

Loss of genetic variability in social spiders: genetic and phylogenetic consequences of population subdivision and inbreeding

The consequences of population subdivision and inbreeding have been studied in many organisms, particularly in plants. However, most studies focus on the short‐term consequences, such as inbreeding depression. To investigate the consequences of both population fragmentation and inbreeding for genetic variability in the longer term, we here make use of a natural inbreeding experiment in spiders, where sociality and accompanying population subdivision and inbreeding have evolved repeatedly. We use mitochondrial and nuclear data to infer phylogenetic relationships among 170 individuals of Anelosimus spiders representing 23 species. We then compare relative mitochondrial and nuclear genetic variability of the inbred social species and their outbred relatives. We focus on four independently derived social species and four subsocial species, including two outbred–inbred sister species pairs. We find that social species have 50% reduced mitochondrial sequence divergence. As inbreeding is not expected to reduce genetic variability in the maternally inherited mitochondrial genome, this suggests the loss of variation due to strong population subdivision, founder effects, small effective population sizes (colonies as individuals) and lineage turnover. Social species have < 10% of the nuclear genetic variability of the outbred species, also suggesting the loss of genetic variability through founder effects and/or inbreeding. Inbred sociality hence may result in reduction in variability through various processes. Sociality in most Anelosimus species probably arose relatively recently (0.1–2 mya), with even the oldest social lineages having failed to diversify. This is consistent with the hypothesis that inbred spider sociality represents an evolutionary dead end. Heterosis underlies a species potential to respond to environmental change and/or disease. Inbreeding and loss of genetic variability may thus limit diversification in social Anelosimus lineages and similarly pose a threat to many wild populations subject to habitat fragmentation or reduced population sizes.     

Genetic population structure, queen supersedure and social polymorphism in a social Hymenoptera

In social insects, the emergence of multiple queening is linked to changes in a suite of traits such as the reproductive life span of queens, mating patterns and population structure. We investigated queen turnover, colony longevity, spatial distribution patterns and genetic differentiation in a population of the socially polymorphic ant Formica fusca. Genetic differentiation between the social forms was absent, and mating patterns were similar in the two forms. The spatial distribution of single- and multi-queen colonies indicated an absence of colony reproduction by budding in both colony types. However, the rate of queen supersedure was high in multi-queen colonies and absent in single-queen ones. The social structure of colonies remained stable across years, but colony mortality did not differ between the two social forms. These results imply that differences between social types may appear and persist also in sympatry, and that these differences may occur in some traits, but not others, despite the presence of homogenizing gene flow.     

Complete separation along matrilines in a social spider metapopulation inferred from hypervariable mitochondrial DNA region

The distribution and quantity of genetic diversity may be profoundly influenced by the emergence and dynamics of social groups. Permanent social living in spiders has resulted in the subdivision of their populations in more or less isolated colony lineages that grow, proliferate and become extinct without mixing with one another. A newly discovered hypervariable mitochondrial DNA region allowed us to examine the fine scale metapopulation structure in the social Anelosimus eximius. We sampled 39 colonies in Ecuador and French Guiana and identified 25 haplotypes. The majority of colonies contained one haplotype. Additional haplotypes occurred in approximately 15% of the colonies, and were always closely related to the common colony haplotype. Our findings confirm that colonies consist of single matrilines, with within‐colony variation explained by mutations within the matriline. We thus found no evidence of mixing of matrilines. Likewise, colonies in a cluster often shared a haplotype, implying common colony ancestry. In few cases, however, haplotypes were shared between more distant colonies, providing evidence for occasional longer distance dispersal and/or widespread colony lineages. The geographical localities of colonies were incongruent with phylogenetic trees and haplotype networks, showing that some areas contained two or more matrilines. Hence, females do not migrate into foreign colonies, but faithfully remain within their own colony lineage, even when they disperse into new areas. These results indicate that the fine scale metapopulation structure of pure matrilines is maintained over the long term and that colony turnover is not extensive or radical enough to homogenize entire geographical areas. Genetic diversity is thus preserved to some extent at the metapopulation level.     

A molecular phylogenetic analysis of reproductive trait evolution in the soft coral genus Alcyonium

The soft coral genus Alcyonium is among the most reproductively diverse invertebrate taxa known: The genus includes species that vary both in mode of reproduction (including broadcast spawners, internal brooders, and external brooders) and sexual expression (gonochores, hermaphrodites, and a unisexual parthenogen). Such diversity offers a unique opportunity to examine associations between reproductive and morphological traits in a phylogenetic context. We used an approximately 900-bp sequence of the nuclear ribosomal gene complex spanning the internal transcribed spacer (ITS) regions to construct a molecular phylogeny for 14 European and North American species of Alcyonium onto which we mapped the known distribution of reproductive and morphological traits. The phylogeny suggests that hermaphroditism or parthenogenesis has evolved independently at least twice in this genus, and always in internally brooding species. Broadcast spawning and external brooding only occur in species with large colony size, whereas all species with small colony size brood their larvae internally. Internal brooding and small size appear to be ancestral in this genus; if this is the case, an association between broadcast spawning and large colony size has evolved independently in at least two clades. This tendency of small adults to brood their larvae while large adults broadcast spawn them into the plankton has been observed in a variety of solitary invertebrate taxa, but to date has not been documented in any other colonial invertebrates. Moreoever, it has been suggested that organisms with a colonial growth form should not experience the allometric constraints on brood space that have been proposed to explain the association between adult size and mode of reproduction in solitary organisms. Unlike many other colonial groups, however, module (polyp) size is strongly correlated with colony size in Alcyonium, and constraints on brooding may be imposed by module, rather than colony, allometry. The very close genetic relationship (< 1% sequence divergence) and shared polymorphisms among A. digitatum (a large, gonochoric broadcast spawner), A. siderium, and A. sp. A (intermediate-sized and small hermaphroditic, internal brooders) suggest that evolutionary transitions between broadcast spawning and brooding and between gonochorism and hermaphroditism can occur easily and rapidly in this group.