Experimental fragmentation reduces sexual reproductive output by the reef-building coral Pocillopora damicornis

Natural and anthropogenic disturbances may fragment stony reef corals, but few quantitative data exist on the impacts of skeletal fragmentation on sexual reproduction in corals. We experimentally fragmented colonies of the branching coral Pocillopora damicornis and determined the number and size of planula larvae released during one lunar reproductive cycle. Partially fragmented colonies significantly delayed both the onset and peak period of planula release compared with intact control colonies. Most fragments removed from the corals died within 11–18 days, and released few planulae. The total number of planulae released per coral colony varied exponentially with remaining tissue volume, and was significantly lower in damaged versus undamaged colonies. However, the number of planulae produced per unit tissue volume, and planula size, did not vary with damage treatment. We conclude that even partial fragmentation of P. damicornis colonies (<25% of tissue removed) decreases their larval output by reducing reproductive tissue volume. Repeated breakage of corals, such as caused by intensive diving tourism or frequent storms, may lead to substantially reduced sexual reproduction. Therefore, reef management should limit human activities that fracture stony corals and lead to decreases in colony size and reproductive output. Accepted: 2 February 2000     

Reproductive strategy, clonal structure and genetic diversity in populations of the aquatic macrophyte Sparganium emersum in river systems

Many aquatic and riparian plant species are characterized by the ability to reproduce both sexually and asexually. Yet, little is known about how spatial variation in sexual and asexual reproduction affects the genotypic diversity within populations of aquatic and riparian plants. We used six polymorphic microsatellites to examine the genetic diversity within and differentiation among 17 populations (606 individuals) of Sparganium emersum, in two Dutch-German rivers. Our study revealed a striking difference between rivers in the mode of reproduction (sexual vs. asexual) within S. emersum populations. The mode of reproduction was strongly related to locally reigning hydrodynamic conditions. Sexually reproducing populations exhibited a greater number of multilocus genotypes compared to asexual populations. The regional population structure suggested higher levels of gene flow among sexually reproducing populations compared to clonal populations. Gene flow was mainly mediated via hydrochoric dispersal of generative propagules (seeds), impeding genetic differentiation among populations even over river distances up to 50 km. Although evidence for hydrochoric dispersal of vegetative propagules (clonal plant fragments) was found, this mechanism appeared to be relatively less important. Bayesian-based assignment procedures revealed a number of immigrants, originating from outside our study area, suggesting intercatchment plant dispersal, possibly the result of waterfowl-mediated seed dispersal. This study demonstrates how variation in local environmental conditions in river systems, resulting in shifting balances of sexual vs. asexual reproduction within populations, will affect the genotypic diversity within populations. This study furthermore cautions against generalizations about dispersal of riparian plant species in river systems.     

Fire coral clones demonstrate phenotypic plasticity among reef habitats

Clonal populations are often characterized by reduced levels of genotypic diversity, which can translate into lower numbers of functional phenotypes, both of which impede adaptation. Study of partially clonal animals enables examination of the environmental settings under which clonal reproduction is favoured. Here, we gathered genotypic and phenotypic information from 3,651 georeferenced colonies of the fire coral Millepora platyphylla in five habitats with different hydrodynamic regimes in Moorea, French Polynesia. In the upper slope where waves break, most colonies grew as vertical sheets (“sheet tree”) making them more vulnerable to fragmentation. Nearly all fire corals in the other habitats are encrusting or massive. The M. platyphylla population is highly clonal (80% of the colonies are clones), while characterized by the highest genotype diversity ever documented for terrestrial or marine populations (1,064 genotypes). The proportion of clones varies greatly among habitats (≥58%–97%) and clones (328 clonal lineages) are distributed perpendicularly from the reef crest, perfectly aligned with wave energy. There are six clonal lineages with clones dispersed in at least two adjacent habitats that strongly demonstrate phenotypic plasticity. Eighty per cent of the colonies in these lineages are “sheet tree” on the upper slope, while 80%–100% are encrusting or massive on the mid slope and back reef. This is a unique example of phenotypic plasticity among reef‐building coral clones as corals typically have wave‐tolerant growth forms in high‐energy reef areas.     

Life in the colonies: learning the alien ways of colonial organisms

Who needs to go to outer space to study alien beings when the oceans of our own planet abound with bizarre and unknown creatures? Many of them belong to sessile clonal and colonial groups, including sponges, hydroids, corals, octocorals, ascidians, bryozoans, and some polychaetes. Their life histories, in many ways unlike our own, are a challenge for biologists. Studying their ecology, behavior, and taxonomy means trying to “think like a colony” to understand the factors important in their lives. Until the 1980s, most marine ecologists ignored these difficult modular organisms. Plant ecologists showed them ways to deal with the two levels of asexually produced modules and genetic individuals, leading to a surge in research on the ecology of clonal and colonial marine invertebrates. Bryozoans make excellent model colonial animals. Their life histories range from ephemeral to perennial. Aspects of their lives such as growth, reproduction, partial mortality due to predation or fouling, and the behavior of both autozooids and polymorphs can be studied at the level of the colony, as well as that of the individual module, in living colonies and over time.     

The role of sexual and asexual reproduction in structuring high latitude populations of the reef coral Pocillopora damicornis

The genotypic composition of populations of the asexually viviparous coral Pocillopora damicornis varies in a manner that challenges classical models of the roles of sexual and asexual reproduction. On the geographically isolated Hawaiian reefs and high latitude reefs in Western Australia, P. damicornis populations are highly clonal although it has been argued that sexual reproduction via broadcast spawning generates widely dispersed colonists. In contrast, on eastern Australia's tropical Great Barrier Reef populations show little evidence of clonality. Here, we compare the genotypic diversity of adult and juvenile colonies of P. damicornis at seven sites on eastern Australia's high latitude Lord Howe Island reefs to determine if levels of clonality vary with habitat heterogeneity and age of colonies (as predicted by theory) or alternatively if clonality is again always high as for other isolated reef systems. We found 55-100% of the genotypic diversity expected for random mating at all seven sites and little evidence of asexual recruitment irrespective of habitat heterogeneity (sheltered versus wave exposed) or colony age. We found reduced levels of genetic diversity compared with tropical reefs (2.75 versus 4 alleles/locus), which supports earlier findings that Lord Howe Island is an isolated reef system. Furthermore, heterozygote deficits coupled with significant genetic subdivision among sites (FST=0.102+/-0.03) is typical of populations that have limited larval connections and are inbred. We conclude that the genetic structure of P. damicornis at Lord Howe Island reflects populations that are maintained through localised recruitment of sexually produced larvae.     

Sexual reproduction,development and larval biology in scleractinian corals

This paper brings together widely scattered information on sexual reproduction in scleractinian corals. It includes a review of information and ideas on sex determination, gametogenesis, gametogenic cycles, fertilization and embryonic development, spawning and planula release, larval behavior, settlement and metamorphosis. The review deals with corals from different habitats and organismic assemblages, including tropical reef corals, temperate water corals, solitary and colonial forms. A summary table of coral species and their known reproductive characteristics is presented.     

Evaluating Methods for Transplanting Endangered Elkhorn Corals in the Virgin Islands

Restoration of rare corals is desirable and restoration projects are fairly common, but scientific evaluation of this approach is limited. We tested several techniques for transplant and restabilization of Acropora palmata (the elkhorn coral), an ecologically important Caribbean coral whose populations have suffered severe declines. In rough weather, fragments break‐off colonies of branching corals like A. palmata as a normal form of asexual reproduction. We transplanted naturally produced coral fragments from remnant populations to nearby restoration sites. Untouched control fragments at the donor site died faster and grew slower than fragments attached to the reef, so attaching fragments to the reef is beneficial. Transplanted fragments grew and died at a rate similar to fragments left at the donor site (both groups were attached to the reef), so there were no effects of moving fragments or differences in habitat quality between donor and restoration sites. Growth and survival were similar using four methods of attaching fragments to the reef: cable ties, two types of epoxy resin, and hydrostatic cement. Corals sometimes compete with the macroalgae that dominate degraded reefs, and clearing surrounding algae improved the growth of fragments. After 4 years, transplanted fragments grew to 1,450 cm² in area and so were potentially sexually active. Because the methods tested are simple and cheap, they could be used by volunteer recreational divers to restore locally extirpated A. palmata populations or to enhance reefs where natural recovery is slow.     

Microgeographic variation in recruitment under adult trees: arrival of new genotypes or perpetuation of the existing ones?

• Investigating spatial variation in the relative importance of sexual reproduction and clonal propagation is critical to obtain more accurate estimates of future effective population sizes and genetic diversity, as well as to identify ecological correlates of clonality.
• We combined a stratified sampling scheme with microsatellite genetic analyses to estimate variation in the proportion of sexual versus clonal recruits among saplings in five populations of the tree Pyrus bourgaeana. Using a likelihood framework, we identified clones among the genotypes analysed and examined variation among populations regarding the proportion of saplings coming from clonal propagation. We also examined the relationship between the relative abundance of clonal shoots across the studied populations and their herbivory levels.
• Our results revealed that one third of the saplings examined (N = 225 saplings) had a probability above 0.9 of being clones of nearby (<10 m) trees, with the ratio between clonal propagation and sexual recruitment varying up to eight‐fold among populations. A small portion of these putative clonal shoots reached sexual maturity. Relative abundance of clonal shoots did not significantly relate to the herbivory by ungulates.
• Our results call into question optimistic expectations of previous studies reporting sufficient levels of recruitment under parental trees without animal seed dispersal services. Nevertheless, given that some of these clonal shoots reach sexual maturity, clonal propagation can ultimately facilitate the long‐term persistence of populations during adverse periods (e.g. environmental stress, impoverished pollinator communities, seed dispersal limitation).

     

The reproductive biology of Polytrichum formosum: clonal structure and paternity revealed by microsatellites

Using highly polymorphic microsatellite markers, we assessed clonal structure and paternity in a population of the bryophyte species Polytrichum formosum. Identical multilocus genotypes of individual shoots were almost never observed in spatially separated cushions, but were found to be highly clustered within moss cushions. Therefore, asexual reproduction through dispersal of gametophyte fragments is not very important in P. formosum. However, asexual reproduction on a very localized scale through vegetative growth of genets (branching of gametophytes via clonal growth of rhizomes) is very extensive. The patchy spatial distribution of genets and the absence of intermingling among genets suggest that this species follows a 'phalanx' clonal growth strategy. Vegetative proliferation of genets will increase their size, and, consequently, will have considerable fitness consequences for individuals in terms of increased genet longevity and reproductive output. Although paternity analysis of sporophytes confirmed male genet size, i.e. gamete production, to be an important determinant of male reproductive fitness, it also showed that the spatial distance to female genets is the predominant factor that governs male reproductive success. Moreover, we showed that male gamete dispersal distances in P. formosum are much further than generally assumed, and are in the order of metres rather than centimetres. Combining the findings, we conclude that the high genotypic diversity observed for this facultatively clonal species is most likely explained by a preponderance of sexual reproduction over clonal reproduction.     

Asexually produced Cape honeybee queens (Apis mellifera capensis) reproduce sexually

Unmated workers of the Cape honeybee Apis mellifera capensis can produce female offspring including daughter queens. As worker-laid queens are produced asexually, we wondered whether these asexually produced individuals reproduce asexually or sexually. We sampled 11 colonies headed by queens known to be the clonal offspring of workers and genotyped 23 worker offspring from each queen at 5 microsatellite loci. Without exception, asexually produced queens produced female worker offspring sexually. In addition, we report the replacement of a queen by her asexually produced granddaughter, with this asexually produced queen also producing offspring sexually. Hence, once a female larva is raised as a queen, mating and sexual reproduction appears to be obligatory in this subspecies, despite the fact that worker-laid queens are derived from asexual lineages.     

EVIDENCE FOR RESTRICTED GENE FLOW IN THE VIVIPAROUS CORAL SERIATOPORA HYSTRIX ON AUSTRALIA'S GREAT BARRIER REEF

Viviparous, branching corals such as Seriatopora hystrix are expected to generate most recruits through asexual reproduction (fission or fragmentation) but are expected to use sexual reproduction to produce widely dispersed colonists. In this study, allozyme electrophoresis was used to test for variation in the relative contributions of sexual and asexual reproduction to recruitment and to assess the apparent scale of larval dispersal (gene flow) in the central Great Barrier Reef. Fifty-seven collections (within ≤ 25 m²) of fragments from sets of approximately 40 colonies were made (where possible) within each of five habitats on each of 12 reefs. These reefs, within the central region of the Great Barrier Reef, were separated by up to 90 km and included one inner-shelf continental island and groups of seven midshelf reefs and four outer-shelf reefs. Most collections contained a high level of multilocus genotypic diversity and hence showed little evidence of recruitment through fragmentation, although the majority of collections displayed large and consistent deficits of heterozygotes. Allele frequencies varied greatly among collections (F_ST = 0.43), and this variation was sufficient to explain two-thirds of observed deficiencies of heterozygotes via a Wahlund effect. A hierarchical assessment of F_ST values revealed that 45% of allelic variation occurred among reefs (F_ST = 0.20), and only 16% of variation within reefs was explained by variation among five major habitat types (F_ST = 0.05). A relatively small component of the total variation among samples was attributable to across-shelf variation among the groups of middle- and outer-shelf reefs (F_ST = 0.03); however, the outer-shelf reefs form a single UPGMA cluster separate from all but 4 of the other 43 collections. These data imply that widespread dispersal does occur but that the direction or magnitude of gene flow may be influenced by the along-shelf movement of major ocean currents and weather-dependent currents on or near reefs. Each reef, therefore, forms a partially isolated and highly subdivided population.     

Asexual and sexual reproductive strategies in clonal plants

Most plants can reproduce both sexually and asexually (or vegetatively),and the balance between the two reproductive modes may vary widely between and within species.Extensive clonal growth may affect the evolution of life history traits in many ways.First,in some clonal species,sexual reproduction and sex ratio vary largely among populations.Variation in sexual reproduction may strongly affect plant's adaptation to local environments and the evolution of the geographic range.Second,clonal growth can increase floral display,and thus pollinator attraction,while it may impose serious constraints and evolutionary challenges on plants through geitonogamy that may strongly influence pollen dispersal.Geitonogamous pollination can bring a cost to plant fitness through both female and male functions.Some co-evolutionary interactions,therefore,may exist between the spatial structure and the mating behavior of clonal plants.Finally,a trade-off may exist between sexual reproduction and clonal growth.Resource allocation to the two reproductive modes may depend on environmental conditions,competitive dominance,life span,and genetic factors.If different reproductive modes represent adaptive strategies for plants in different environments,we expect that most of the resources should be allocated to sexual reproduction in habitats with fluctuating environmental conditions and strong competition,while clonal growth should be dominant in stable habitats.Yet we know little about the consequence of natural selection on the two reproductive modes and factors which control the balance of the two reproductive modes.Future studies should investigate the reproductive strategies of clonal plants simultaneously from both sexual and asexual perspectives.     

Sexual reproduction of Acropora reef corals at Moorea, French Polynesia

Little information is available on reproductive processes among corals in isolated central Pacific reef regions, including French Polynesia. This study examined the timing and mode of sexual reproduction for Acropora reef corals at Moorea. Spawning was observed and/or inferred in 110 Acropora colonies, representing 12 species, following full moon periods in September through November 2002. Gamete release was observed and inferred in four species of Acropora between 9 and 13 nights after the full moon (nAFM) in September 2002. Twelve Acropora spp. spawned gametes between 5 and 10 nAFM in October 2002, with six species spawning 7 nAFM and four species spawning 9 nAFM. In November 2002, spawning of egg and sperm bundles was observed and inferred in 27 colonies of Acropora austera, 6 nAFM. These are the first detailed records of spawning by Acropora corals in French Polynesia.     

Constraints on the formation of colonies of the extant azooxanthellate scleractinian coral Dendrophyllia arbuscula

Sentoku, A. & Ezaki, Y. 2011: Constraints on the formation of colonies of the extant azooxanthellate scleractinian coral Dendrophyllia arbuscula. Lethaia, Vol. 45, pp. 62–70. Scleractinia display a variety of growth forms, whether zooxanthellate or azooxanthellate, as the consequence of the combined effects of both intrinsic and extrinsic factors. New modules arise in colonial corals through asexual reproduction, including budding and division. The azooxanthellate, branching dendrophylliid Dendrophyllia arbuscula van der Horst 1922 , is a good species to investigate intrinsic regularities in budding, because: (1) the lateral corallites always occur in the vicinity of four primary septa, excluding the two directive primary septa; (2) the two directive septa in lateral corallites tend to be oriented almost perpendicular to the growth orientation of parental corallites; (3) the lateral corallites grow more‐or‐less diagonally upwards; and (4) these regularities are retained from the axial to the derived lateral corallites during colony growth. Accordingly, a colony of apparently complex dendroid corals is formed according to certain universal rules that apply to successive generations of corallites. The presence of two opposite sectors in which budding do not occur seems to be common to other azooxanthellate scleractinian families. Regularities, other than the orientation of the directive septa, are also commonly found at least in other azooxanthellate dendrophylliid genera. These regularities suggest the presence of strict developmental constraints on the asexual reproduction of the Scleractinia, both extant and extinct. These regularities by azooxanthellate scleractinians, as one of the representative colonial metazoan groups, provide us with fundamental data with which we can understand how colonies are constructed. □Azooxanthellate coral, budding, colony, Dendrophyllia arbuscula, regularity.     

Intraspecific competition in a reef coral: effects on growth and reproduction

Summary Growth rates and reproduction of a branching coral (Stylophora pistillata) were compared in the presence and in the absence of intraspecific competition. Field experiments demonstrated a significant decline in the growth rate of competing colonies compared to noncompeting control colonies; the growth rate slowed in all of the interacting individuals, irrespective of their place in the hierarchy of the intraspecific dominance or of their color morph. In case of immediate killing of the subordinate, the dominant colony grew at a normal rate. In addition to the marked decrease in the growth rate of interacting colonies, the typical symmetry shape of these colonies was changed to an abnormal growth form. The number of female gonads per polyp was significantly reduced in colonies competing intraspecifically, and the typical synchrony in reproduction among different branches of a given colony was changed and desynchronized. Again, these results did not correlate with the hierarchy of dominance. We conclude that intraspecific competition in reef corals involves great investment of energy. The ecological significance and the different pathways of this competition are discussed.     

Storm cycles in the last millennium recorded in Yongshu Reef, southern South China Sea

Large storm-relocated Porites coral blocks are widespread on the reef flats of Nansha area, southern South China Sea. Detailed investigations of coral reef ecology, geomorphology and sedimentation on Yongshu Reef indicate that such storm-relocated blocks originated from large Porites lutea corals growing on the spurs within the reef-front living coral zone. Because the coral reef has experienced sustained subsidence and reef development during the Holocene, dead corals were continuously covered by newly growing coral colonies. For this reason, the coral blocks must have been relocated by storms from the living sites and therefore the ages of these storm-relocated corals should approximate the times when the storms occurred. Rapid emplacement of these blocks is also evidenced by the lack of coral overgrowth, encrustation or subtidal alteration.U-series dating of the storm-relocated blocks as well as of in situ reef flat corals suggests that, during the last 1000 years, at least six strong storms occurred in 1064±30, 1210±5-1201±4, 1336±9, 1443±9, 1685±8-1680±6, 1872±15 AD, respectively, with an average 160-year cycle (110-240 years). The last storm, which occurred in 1872±15 AD, also led to mortality of the reef flat corals dated at ∼130 years ago. Thus, the storm had significant impacts on coral reef ecology and morphology.     

Genetic relatedness does not retain spatial pattern across multiple spatial scales: dispersal and colonization in the coral,Pocillopora damicornis

Patterns of isolation by distance are uncommon in coral populations. Here, we depart from historical trends of large‐scale, geographical genetic analyses by scaling down to a single patch reef in Kāne‘ohe Bay, Hawai‘i, USA, and map and genotype all colonies of the coral, Pocillopora damicornis. Six polymorphic microsatellite loci were used to assess population genetic and clonal structure and to calculate individual colony pairwise relatedness values. Our results point to an inbred, highly clonal reef (between 53 and 116 clonal lineages of 2352 genotyped colonies) with a much skewed genet frequency distribution (over 70% of the reef was composed of just seven genotypes). Spatial autocorrelation analyses revealed that corals found close together on the reef were more genetically related than corals further apart. Spatial genetic structure disappears, however, as spatial scale increases and then becomes negative at the largest distances. Stratified, random sampling of three neighbouring reefs confirms that reefs are demographically open and inter‐reef genetic structuring was not detected. Attributing process to pattern in corals is complicated by their mixed reproductive strategies. Separate autocorrelation analyses, however, show that the spatial distribution of both clones and nonclones contributes to spatial genetic structure. Overall, we demonstrate genetic structure on an intrareef scale and genetic panmixia on an inter‐reef scale indicating that, for P. damicornis, the effect of small‐ and large‐scale dispersal processes on genetic diversity are not the same. By starting from an interindividual, intrareef level before scaling up to an inter‐reef level, this study demonstrates that isolation‐by‐distance patterns for the coral P. damicornis are limited to small scales and highlights the importance of investigating genetic patterns and ecological processes at multiple scales.     

New insights into the dynamics between reef corals and their associated dinoflagellate endosymbionts from population genetic studies

The mutualistic symbioses between reef‐building corals and micro‐algae form the basis of coral reef ecosystems, yet recent environmental changes threaten their survival. Diversity in host‐symbiont pairings on the sub‐species level could be an unrecognized source of functional variation in response to stress. The Caribbean elkhorn coral, Acropora palmata, associates predominantly with one symbiont species (Symbiodinium ‘fitti’), facilitating investigations of individual‐level (genotype) interactions. Individual genotypes of both host and symbiont were resolved across the entire species’ range. Most colonies of a particular animal genotype were dominated by one symbiont genotype (or strain) that may persist in the host for decades or more. While Symbiodinium are primarily clonal, the occurrence of recombinant genotypes indicates sexual recombination is the source of this genetic variation, and some evidence suggests this happens within the host. When these data are examined at spatial scales spanning the entire distribution of A. palmata, gene flow among animal populations was an order of magnitude greater than among populations of the symbiont. This suggests that independent micro‐evolutionary processes created dissimilar population genetic structures between host and symbiont. The lower effective dispersal exhibited by the dinoflagellate raises questions regarding the extent to which populations of host and symbiont can co‐evolve during times of rapid and substantial climate change. However, these findings also support a growing body of evidence, suggesting that genotype‐by‐genotype interactions may provide significant physiological variation, influencing the adaptive potential of symbiotic reef corals to severe selection.     

Survival of hurricane-generated coral fragments and a disturbance model of reef calcification/growth rates

Summary Hurricane Gerta, with winds reaching 150 km/h, crossed the Belize barrier reef on September 18, 1978. Breakage and scouring of corals occurred in all zones of the reef to a depth of approximately 25 m. Survivorship of storm-generated coral fragments and detached colonies is strongly size dependent, conforming to the power function Y=4.44X^0.66 where Y is the percent of fragments and X is the fragment size. Forty-six percent of detached Acropora palmata branches, which are larger ( =37.6 cm long) than fragments of other species ( =16.7 cm long), survived. Overall, 39% of fragments and detached colonies survived. This high survivorship, which probably increased the total number of colonies present, and redistribution of corals may explain the rapid recovery of reefs from all but the severest hurricanes. Storms appear to prevent coral reefs from reaching a mature state characterized by low calcification and growth rates. Therefore, we suggest that long-term reef calcification and growth rates are highest on reefs periodically distrubed by storms of intermediate intensity.Smithsonian Tropical Research Institute, Box 2072, Balboa, Republic of Panama     

MODES OF REPRODUCTION IN RECENT AND FOSSIL CUPULADRIID BRYOZOANS

Abstract:  Cupuladriid cheilostome bryozoans can make new colonies both sexually and asexually. Sexual (aclonal) colonies are derived from larvae while asexual (clonal) colonies result from the fragmentation or division of larger colonies. A number of specialised morphologies exist which either enhance or discourage clonality, and cupuladriids preserve these in their skeletons, meaning that it is possible to count the abundances of individual modes of reproduction in fossil assemblages, and thus measure the mode and tempo of evolution of life histories using fossil colonies. In this paper we categorise, illustrate and describe the various clonal and aclonal methods of propagation in cupuladriids through the Cenozoic. Sexual reproduction is the only aclonal method of propagation, while four clonal methods are described comprising: (1) mechanical fragmentation, (2) autofragmentation, (3) colonial budding and (4) peripheral fragmentation. The processes involved in each are discussed and we explain how their prevalence can be measured in the fossil record using preservable morphologies. Compiling a record of the occurrence and distribution of the various modes of propagation through time and space we discover a general trend of evolution towards more complex modes in all three cupuladriid genera, but a geologically recent extinction of some modes of propagation that has left the present-day assemblage relatively depauperate. We see striking similarities in the general timing of expansion of modes of reproduction between the two most important genera, Cupuladria and Discoporella , although it is clear that Discoporella evolved a much wider range of special morphologies either to enhance or to discourage clonality than did Cupuladria .