Evolution Of Reproductive Strategies Research Articles

A Single‐Cell Atlas of Crab Ovary Provides New Insights Into Oogenesis in Crustaceans

AbstractOogenesis is crucial for sexual reproduction and provides the material basis for population continuation. Nonetheless, the identity of the cells involved, the nature of transformation, and underlying regulators of oogenesis in crustaceans remain elusive. Here, an atlas of the ovary is plotted via single‐nuclei RNA sequencing (snRNA‐seq) in the mud crab Scylla paramamosain, resulting in five cell types, including germ cells, somatic cells, and three follicle cell types identified, which in turn provides abundant candidate markers for them. Moreover, profiles of ligand‐receptor in different cells of the crab ovary indicate the roles of cell communication in oogenesis. Dozens of transcription factors in the trajectory from oogonia to oocytes as well as the key molecules/pathways in somatic cells and follicle cells relevant to oogenesis are screened, which is evolutionarily conserved and its underlying regulatory mechanism is subject to some modification across various phyla. The spatiotemporal expression patterns of seven markers are further verified and the RNAi confirms the essential roles of piwi and VgR in oogenesis. These data help to elucidate the mechanism underlying gametogenesis and the evolution of reproductive strategy in invertebrates.

The nature of nurture: Darwinian and mendelian perspectives.

Two perspectives on the nature of nurture are reviewed, one Mendelian and the other Darwinian, in an effort to draw links between the two and, thereby, integrate them in a developmental modern synthesis, mirroring the one that took place in biology early in the last century. Thus, the heritability of environmental measures and gene-X-environment interaction are discussed with respect to Mendelian nature before turning attention to Darwinian nature and thus the development of reproductive strategies and differential susceptibility to environmental influences. Conclusions are drawn with respect to both frameworks indicating that it is time to abandon the biology-is-destiny resistance to both approaches to studying and thinking about development, especially when it comes to the nature of nurture. Implications for the future development of the field of developmental psychopathology are highlighted.

The interplay between climatic niche evolution, polyploidy and reproductive traits explains plant speciation in the Mediterranean Basin: a case study in Centaurium (Gentianaceae).

Speciation and diversification patterns in angiosperms are frequently shaped by niche evolution. Centaurium Hill is a Mediterranean genus with ca. 25 species, of which 60% are polyploids (tetra- and hexaploids), distributed mainly in the Mediterranean Basin and in areas with temperate and arid climates of Asia, Europe, North-Central Africa and North America. The evolutionary history of this genus has been studied using morphological, biogeographical and molecular approaches, but its climatic niche characterization and its relation with genome evolution (chromosome number and ploidy level) has not been addressed yet. Thus, this study aims to identify the role of the evolution of climatic niche, ploidy level, life cycle and floral traits in the diversification of Centaurium. Climatic niche characterization involved estimating present climate preferences using quantitative data and reconstructing ancestral niches to evaluate climatic niche shifts. The evolution of climatic niche towards selective optima determined by ploidy level (three ploidy levels) and different binary traits (polyploidy, floral size, floral display, herkogamy and life cycle) was addressed under the Ornstein-Uhlenbeck model. Chromosome number evolution was inferred using the ChromoSSE model, testing if changes are clado- or anagenetic. Chromosome number evolution and its link with cladogenesis, life cycle and floral traits was modeled on the phylogeny. The reconstruction of the ancestral niches shows that Centaurium originated in a mild climate and diversified to both humid and cold as well as to dry and warmer climates. Niche conservatism was estimated in the climatic niche of the ancestors, while the climatic niche of the current taxa experienced transitions from their ancestors' niche. Besides, the evolution of climatic niche towards multiple selective optima determined by the studied traits was supported, life cycle optima receiving the highest support. The reconstruction of chromosome number transitions shows that the rate of speciation process resulting from chromosomal changes (chromosomal cladogenesis) is similar to that of non-chromosomal cladogenesis. Additionally, dependent evolution of floral size, floral display and herkogamy with chromosome number variation was supported. In conclusion, polyploidization is a crucial process in the Mediterranean region that assisted speciation and diversification into new areas with different climates, entailing niche shifts and evolution of reproductive strategies.

Gametophytic self-incompatibility in Maxillariinae orchids.

Gametophytic self-incompatibility (GSI) has been mainly described in species-rich clades within Orchidaceae. We report GSI for a genuswithin Maxillariinae, one of the most conspicuous and diverse subtribes of neotropical orchids. Here, we describe the reproductive system of Brasiliorchis picta, B. phoenicanthera, and B. porphyrostele. Anatomical studies of fruit development showed that pollen tubes of aborted, self-pollinated flowers degenerate half-way in the stylar channel and never reach the ovules. Spontaneous self-pollination and emasculation set no fruits for none of the sampled species, thus supporting the hypothesis that thesethree species studied rely on the agency of pollinators and pollinator-mediated cross-pollination to set fruit. Fruit set from cross-pollinations ranged from 33.4 to 77.5%. One self-pollinated fruit of B. porphyrostele developed to completion. All other fruits aborted between 10 and 21 days after pollination. These data support previous evidence of variable strength GSI being exhibited in orchid species. Additional studies of self-incompatibility systems are needed to evaluate their role in species diversification and evolution of reproductive strategies in Maxillariinae and to allow for effective conservation strategies of threatened orchid species.

Unexpected morphological variability in the eggshells of the South American caimans Caiman latirostris and Caiman yacare

Eggshell morphology is a valuable indicator of the local conditions within the nests of modern crocodilians and birds. In contrast to these latter, the anatomical structure of the eggshells of most crocodilian species is practically unknown. Here, we provide the first characterization of crocodilian eggshells, using x-ray micro-CT scans. We studied eggshells of Caiman latirostris and Caiman yacare from various developmental stages that coincide with the beginning of embryonic ossification. The new 3D renderings revealed complex ornamentation, unique among crocodilians, and amphora-shaped pore canals, some of which converge in single pore openings. We also documented a high density of pore canals with a gas diffusion capacity 45 times higher than the average predicted for modern avian eggshells. The external ornamentation and the thickness of the compact layer of the eggshells (i.e. excluding ornamentation) showed ontogenetic and interspecific differences that could be related to nesting materials and nesting areas selected by each species. The shell features described here evidence a greater structural complexity than previously recognized in phylogenetically close, sympatric crocodilian species. Further comprehensive morphological analyses on other modern and fossil crocodilian eggshells using micro-CT technology will shed new light on the evolution of reproductive strategies in this intriguing archosaur clade.

Confocal Laser Scanning Microscopy Applied to a New Species Helps Understand the Functioning of the Reproductive Apparatus in Stylet-Bearing Urodasys (Gastrotricha: Macrodasyida)

Gastrotrichs are highly diverse and abundant in all aquatic ecosystems; however, they are often overlooked. During a biodiversity survey in Sardinia (Italy), a new species of gastrotrich herein described was discovered. Specimens of Urodasys bifidostylis sp. nov. were found in sandy sediments from two submarine caves. Using an integrative approach of traditional light (DIC) and high-resolution (CLSM) microscopies, we herein reveal, for the first time, the fine structure and function of the reproductive organ in an Urodasys representative. This is particularly relevant considering the complex reproductive organs and strategies of this group. Results allow comparisons between the reproductive apparatus and sperm transfer modalities in Urodasys and the closely related genus Macrodasys. One similarity is that both groups transfer male gametes in packets, suggesting the production of spermatophores to be a common phenomenon in Gastrotricha. Unique to Urodasys is the ability of multiple and consecutive copulations and sperm transfers and, differently than Macrodasys, the transfer of sperms unlikely occurs simultaneously between the two hermaphroditic partners. These findings provide new insights into the reproductive strategies of Urodasys and are expected to advance future studies on the evolution of reproductive strategies and the rise of interspecific reproductive barriers in interstitial meiofauna.

MASTREE+: Time-series of plant reproductive effort from six continents.

Significant gaps remain in understanding the response of plant reproduction to environmental change. This is partly because measuring reproduction in long‐lived plants requires direct observation over many years and such datasets have rarely been made publicly available. Here we introduce MASTREE+, a data set that collates reproductive time‐series data from across the globe and makes these data freely available to the community. MASTREE+ includes 73,828 georeferenced observations of annual reproduction (e.g. seed and fruit counts) in perennial plant populations worldwide. These observations consist of 5971 population‐level time‐series from 974 species in 66 countries. The mean and median time‐series length is 12.4 and 10 years respectively, and the data set includes 1122 series that extend over at least two decades (≥20 years of observations). For a subset of well‐studied species, MASTREE+ includes extensive replication of time‐series across geographical and climatic gradients. Here we describe the open‐access data set, available as a.csv file, and we introduce an associated web‐based app for data exploration. MASTREE+ will provide the basis for improved understanding of the response of long‐lived plant reproduction to environmental change. Additionally, MASTREE+ will enable investigation of the ecology and evolution of reproductive strategies in perennial plants, and the role of plant reproduction as a driver of ecosystem dynamics.

Fruit heteromorphism and germination success in the perennial shrub tithonia diversifolia (Asteraceae)

Studies of fruit or seed heteromorphism (the presence of two or more fruit or seed morphs within an individual) provide valuable information about the influence of environmental variation on the evolution of reproductive strategies. Such heteromorphisms are more likely to be favoured by selection in annual species, because short-lived plants are in a disadvantaged position to gather information about environmental conditions their offspring are likely to face when they germinate, compared with perennial counterparts. Here, we describe fruit heteromorphism of Tithonia diversifolia, a perennial shrub found in habitats with contrasting environmental conditions. We tested whether fruit morphs differ in weight and germination success, and whether populations differed in fruit morph ratio. To do this, we first determined fruit morph ratio of three populations from contrasting ecosystems (evergreen high forest, evergreen medium forest and oak-pine forest), and compared germination success in a common-garden setting. In all populations, two fruit morphs were consistently distinguishable within the same capitulum. Although fruit morph ratios differed significantly across populations. Furthermore, fruit morphs differed in weight and germination success, but the direction of the difference was dependent on the population. These results suggest that fruit heteromorphism in the perennial T. diversifolia might represent distinct reproductive strategies allowing it to adapt to uncertain environmental conditions.

Spatial distribution of oncocerid cephalopods on a Middle Devonian bedding plane suggests semelparous life cycle

Reproductive strategies of extinct organisms can only be recognised indirectly and hence, they are exceedingly rarely reported and tend to be speculative. Here, we present a mass-occurrence with common preservation of pairs of late Givetian (Middle Devonian) oncocerid cephalopods from Hamar Laghdad in the Tafilalt (eastern Anti-Atlas, Morocco). We analysed their spatial occurrences with spatial point pattern analysis techniques and Monte Carlo simulations; our results shows that the pairwise clustering is significant, while ammonoids on the same bedding plane reveal a more random distribution. It is possible that processes such as catastrophic mass mortality or post-mortem transport could have produced the pattern. However, we suggest that it is more likely that the oncocerids were semelparous and died shortly after mating. These findings shed new light on the variation and evolution of reproductive strategies in fossil cephalopods and emphasise that they cannot be based on comparisons with extant taxa without question.

Biología reproductiva de <i>Boana pulchella</i> y <i>Boana punctata</i> (Anura: Hylidae) en poblaciones simpátricas de humedales templados

Boana pulchella habita principalmente climas templados y B. punctata principalmente climas tropicales, lo que permitiría suponer la presencia de estrategias reproductivas diferentes, aún en la región en la que sus poblaciones son simpátricas. En el presente estudio se analizaron y compararon los ciclos reproductivos, parámetros reproductivos y desarrollo de cuerpos grasos (CG) de Boana pulchella y B. punctata en humedales templados del río Paraná Medio. Boana pulchella presentó óvulos maduros de marzo a diciembre. En machos no hubo variación del volumen testicular a lo largo del año y el mayor desarrollo de CG de los machos se observó en invierno. Esta especie presentó un patrón reproductivo continuo. La vitelogénesis de B. punctata se inició en enero, alcanzando el mayor desarrollo ovárico en febrero (verano) y decreciendo hacia mayo (otoño). Los machos presentaron crecimiento testicular en verano, decreciendo hacia otoño y los CG presentaron su máximo desarrollo en enero para ambos sexos. Esta especie mostró un patrón reproductivo continuo. Ambas especies presentaron dimorfismo sexual con hembras que poseen una relación proporcional entre la talla y la inversión reproductiva. Boana pulchella presentó un mayor esfuerzo reproductivo (ER = 20,48 ± 12,9) y factor de tamaño ovárico (FTO = 25,73) que B. punctata (ER = 10,06 ± 4,45; FTO = 8,99). También se encontraron diferencias interespecíficas en la masa ovárica, complemento ovárico y volúmen testicular, siendo estas variables proporcionalmente mayores en B. pulchella. Las diferencias observadas en las poblaciones simpátricas podrían relacionarse con el desarrollo de estrategias reproductivas bajo diferentes presiones evolutivas.Material suplementario: https://doi.org/10.15446/caldasia.v41n2.80604

High indirect fitness benefits for helpers across the nesting cycle in the tropical paper wasp Polistes canadensis.

Explaining the evolution of helping behaviour in the eusocial insects where nonreproductive ("worker") individuals help raise the offspring of other individuals ("queens") remains one of the most perplexing phenomena in the natural world. Polistes paper wasps are popular study models, as workers retain the ability to reproduce: such totipotency is likely representative of the early stages of social evolution. Polistes is thought to have originated in the tropics, where seasonal constraints on reproductive options are weak and social groups are effectively perennial. Yet, most Polistes research has focused on nontropical species, where seasonality causes family groups to disperse; cofoundresses forming new nests the following spring are often unrelated, leading to the suggestion that direct fitness through nest inheritance is key in the evolution of helping behaviour. Here, we present the first comprehensive genetic study of social structure across the perennial nesting cycle of a tropical Polistes-Polistes canadensis. Using both microsatellites and newly developed single nucleotide polymorphism markers, we show that adult cofoundresses are highly related and that brood production is monopolized by a single female across the nesting cycle. Nonreproductive cofoundresses in tropical Polistes therefore have the potential to gain high indirect fitness benefits as helpers from the outset of group formation, and these benefits persist through the nesting cycle. Direct fitness may have been less important in the origin of Polistes sociality than previously suggested. These findings stress the importance of studying a range of species with diverse life history and ecologies when considering the evolution of reproductive strategies.

Offspring mass variation in tree swallows: A case of bet-hedging?

The evolution of reproductive strategies is affected by the ability of organisms to deal with future environmental conditions. When environments are temporally unpredictable, however, it is difficult to anticipate optimal offspring phenotype. Diversification of offspring phenotypes, a strategy called diversified bet‐hedging, may allow parents to maximize their fitness by reducing between‐year variation in reproductive success. The link between diversification of offspring phenotypes and individual reproductive success, however, has rarely been documented empirically. We used an eight‐year dataset (1215 broods, 870 females) on individually marked tree swallows (Tachycineta bicolor) to assess whether intra‐brood mass variation was compatible with a diversified bet‐hedging strategy. Intra‐brood mass variation was weakly, but significantly repeatable within females, suggesting consistent individual differences. Greater intra‐brood mass variation, however, was not associated with reduced between‐year variation in reproductive success or increased female reproductive success. Moreover, contrary to diversified bet‐hedging expectations, fledging success of large broods was greater when hatchlings had similar rather than variable masses. Our results suggest that intra‐brood mass variation may not result from diversified bet‐hedging, but rather from complex interactions between environmental, brood, and maternal characteristics.

Joint effects of group sex-ratio and Wolbachia infection on female reproductive success in the terrestrial isopod Armadillidium vulgare

BackgroundIn species that reproduce with sexual reproduction, males and females often have opposite strategies to maximize their own fitness. For instance, males are typically expected to maximize their number of mating events, whereas an excessive number of mating events can be costly for females. Although the risk of sexual harassment by males and resulting costs for females are expected to increase with the proportion of males, it remains unknown whether and how parasitic distorters of a host population’s sex-ratio can shape this effect on the fitness of females. Here, we addressed this question using Armadillidium vulgare and its parasite Wolbachia that alters the sex-ratio of a population. We set up Wolbachia-free and Wolbachia-infected females in experimental groups exhibiting 100, 80, 50% or 20% females for 1 year, during which we measured changes in survival, fertility and fecundity.ResultsWolbachia infection shaped the effects of both population sex-ratio and reproductive season on female fecundity. Compared to Wolbachia-free females, Wolbachia-infected females were less likely to be gravid in populations exhibiting an excess of females and did not exhibit the otherwise negative effect of seasons on this likelihood. Group sex-ratio and Wolbachia infection have independent effects on other measured traits. Male-biased populations had females both exhibiting the lowest survival rate after 6 months and producing the smallest number of offspring, independent of Wolbachia infection. Conversely, Wolbachia-infected females had the lowest likelihood of producing at least one offspring, independent of group sex-ratio. Wolbachia infection had no effect on female survival rate.ConclusionsWe demonstrated that male-biased sex-ratio and the presence of Wolbachia are costly for females due to sexual harassment by males and bacterial infection, respectively. Interestingly, Wolbachia infection triggers another negative effect. This effect does not come from an excess of males and its associated sexual harassment of females but instead from a lack of males and the associated risk for females of remaining unmated. Overall, these findings highlight the importance of social pressures and infection on female fitness and provide insights into our general understanding of the joint and opposite effects of these two parameters in the evolution of reproductive strategies.

Transcriptome characterization of male accessory glands in ants to identify molecules involved in their reproductive success.

In insects, seminal fluid proteins that are produced by male accessory glands and transferred to females during mating have key functions in sperm competition and sperm physiology that lead to male reproductive success. In ants, male reproductive success also depends on the longevity of sperm stored in the queen's spermatheca because their sexual offspring are usually produced only after a prolonged storage period. We identified genes that were up-regulated in the male accessory glands relative to the bodies of Crematogaster osakensis to characterize the reproductive molecules associated with male reproductive success in ants. We found novel genes that had no hits in a homology search and that were predominantly expressed in the accessory glands. These reproductive proteins may have evolved under rapid positive selection for reproductive success in the species. Furthermore, we discovered that three spermatheca-specific genes of C.osakensis queens were also enriched in the accessory glands relative to the bodies of males. These genes may be important for maintaining the sperm quality continuously from ejaculation by males to prolonged storage by queens. This research provides crucial information about the molecular mechanisms of sperm maintenance and sexual selection in ants, and also insight into the evolution of reproductive strategies in insects.

Mechanisms underlying maternal care in a viviparous snake, Sistrurus miliarius: Does maternal body condition, corticosterone, or arginine vasotocin mediate post-birth maternal investment?

The level of parental investment in free-living offspring varies greatly within and among vertebrate taxa, and the mechanisms that mediate investment are likely targets of selection in the evolution of reproductive strategies. In mammalian and avian systems, individual investment is adjusted according to parental energetic status, and regulatory mechanisms have been described. Parental care is also a component of the life history of several groups of squamates and archosaurs, but little to nothing is known regarding the mechanisms that underlie individual variation in parental investment in these groups. Therefore, we examined the relationships among maternal body condition, corticosterone, arginine vasotocin (AVT), and maternal care in postparturient pigmy rattlesnakes. Energetic status was manipulated in pregnant females by supplemental feeding, and AVT was manipulated in postparturient mothers by intraperitoneal injection. Circulating corticosterone and body condition were recorded in postparturient mothers. Mother-offspring spatial relationships were analyzed to determine the closeness of mother-offspring associations. No significant relationship between maternal body condition and baseline corticosterone was observed in mothers, and no significant relationship was found between corticosterone and the level of maternal association with offspring. Manipulation of AVT did not stimulate maternal care. There was a strong and repeatable positive relationship between maternal postparturient body condition and the level of maternal association with offspring. The lack of a significant correlation between body condition and corticosterone does not support the hypothesis that a postparturient glucocorticoid response drives the observed condition-dependence of maternal offspring association.

Cephalopod embryonic shells as a tool to reconstruct reproductive strategies in extinct taxa.

An exhaustive study of existing data on the relationship between egg size and maximum size of embryonic shells in 42 species of extant cephalopods demonstrated that these values are approximately equal regardless of taxonomy and shell morphology. Egg size is also approximately equal to mantle length of hatchlings in 45 cephalopod species with rudimentary shells. Paired data on the size of the initial chamber versus embryonic shell in 235 species of Ammonoidea, 46 Bactritida, 13 Nautilida, 22 Orthocerida, 8 Tarphycerida, 4 Oncocerida, 1 Belemnoidea, 4 Sepiida and 1 Spirulida demonstrated that, although there is a positive relationship between these parameters in some taxa, initial chamber size cannot be used to predict egg size in extinct cephalopods; the size of the embryonic shell may be more appropriate for this task. The evolution of reproductive strategies in cephalopods in the geological past was marked by an increasing significance of small-egged taxa, as is also seen in simultaneously evolving fish taxa.

Effect of Resource Reallocation on Pollen Limitation and Reproductive Assurance of Apocynum venetum L. in an Arid Region

<p>Pollen limitation is considered to be a strong force driving the evolution of reproductive strategies in flowering plants. However, resource reallocation may occur among seeds because of variation in the quantity or quality of pollen received. We performed single-flower and whole-plant pollen supplementation and emasculation of flowers of <em>Apocynum venetum</em> L. to estimate pollen limitation and reproductive assurance. In addition, we calculated the visiting patterns of the pollinators, frequency of pollinators to estimate the effect of pollinator activity and further on the reproductive success of <em>A. venetum</em>. Our results indicated estimates from single-flower manipulations were not biased, closely resembling those from whole-plant manipulations. We found<em> Apis mellifera</em> was the dominant pollinator during the pollination process. In addition, insect pollination played a more important role in the outcrossing system, which could explain the differences in reproductive success. Our results also showed that autonomous self-pollination eliminates pollen limitation and provides reproductive assurance.</p>

The decline in fitness with inbreeding: evidence for negative dominance-by-dominance epistasis in Drosophila melanogaster.

Genetic interactions can play an important role in the evolution of reproductive strategies. In particular, negative dominance-by-dominance epistasis for fitness can theoretically favour sex and recombination. This form of epistasis can be detected statistically because it generates nonlinearity in the relationship between fitness and inbreeding coefficient. Measures of fitness in progressively inbred lines tend to show limited evidence for epistasis. However, tests of this kind can be biased against detecting an accelerating decline due to line losses at higher inbreeding levels. We tested for dominance-by-dominance epistasis in Drosophila melanogaster by examining viability at five inbreeding levels that were generated simultaneously, avoiding the bias against detecting nonlinearity that has affected previous studies. We find an accelerating rate of fitness decline with inbreeding, indicating that dominance-by-dominance epistasis is negative on average, which should favour sex and recombination.

Heterogeneity in reproductive success explained by individual differences in bite rate and mass change

Allocation of resources to current reproduction may reduce future reproduction, growth, and survival, but individual heterogeneity in resource acquisition may obscure this fitness cost. In capital breeders, heterogeneity in reproductive success is often related to body mass or condition, underlining the importance of stored reserves for reproduction. Heterogeneity in the rate of resource acquisition could also affect reproduction. Resource acquisition depends on food intake, but the effects of individual foraging rate on mass gain and reproductive success in wild herbivorous mammals are unknown. We measured how individual bite rate affected mass change and reproductive success of 55 female eastern gray kangaroos (Macropus giganteus) over 2 years. Females with faster bite rate had greater subsequent mass gain, leading to greater offspring survival. In one of 2 years, bite rate directly increased juvenile survival to 8 months. Bite rate appeared to have a direct effect on survival to weaning for young born to females with above-average mass gain, particularly for females in better body condition. Independent of bite rate, individual mass change explained most of the variation in offspring survival. We found a weak positive effect of body condition on reproductive success, suggesting that condition affected reproductive success through its effect on mass change and bite rate. Kangaroos appeared to combine income and capital breeding strategies to deal with internal and external constraints on resource allocation. Our study underlines the importance of accounting for different sources of individual heterogeneity that may affect trade-offs among life-history traits, with important consequences for population dynamics and the evolution of reproductive strategies.

Spatial niche facilitates clonal reproduction in seed plants under temporal disturbance.

The evolutionary origins and advantages of clonal reproduction relative to sexual reproduction have been discussed for several taxonomic groups. In particular, organisms with a sessile lifestyle are often exposed to spatial and temporal environmental fluctuations. Thus, clonal propagation may be advantageous in such fluctuating environments, for sessile species that can reproduce both sexually and clonally. Here we introduce the concept of niche to a lattice space that changes spatially and temporally, by incorporating the compatibility between the characteristics of a sessile clonal plant with its habitat into a spatially explicit individual-based model. We evaluate the impact of spatially and temporally heterogeneous environments on the evolution of reproductive strategies: the optimal balance between seed and clonal reproduction of a clonal plant. The spatial niche case with local habitats led to avoidance of specialization in reproductive strategy, whereas stable environments or intensive environmental change tended to result in specialization in either clonal or seed reproduction under neutral conditions. Furthermore, an increase in spatial niches made clonal reproduction advantageous, as a consequence of competition among several genets under disturbed conditions, because a ramet reached a favorable habitat through a rare long-distance dispersal event via seed production. Thus, the existence of spatial niches could explain the advantages of clonal propagation.