Molecular phylogenetics of Melastomataceae and Memecylaceae: implications for character evolution

Melastomataceae are among the most abundant and diversified groups of plants throughout the tropics, but their intrafamily relationships and morphological evolution are poorly understood. Here we report the results of parsimony and maximum likelihood (ML) analyses of cpDNA sequences from the rbcL and ndhF genes and the rpl16 intron, generated for eight outgroups (Crypteroniaceae, Alzateaceae, Rhynchocalycaceae, Oliniaceae, Penaeaceae, Myrtaceae, and Onagraceae) and 54 species of melastomes. The sample represents 42 of the family's currently recognized ～150 genera, the 13 traditional tribes, and the three subfamilies, Astronioideae, Melastomatoideae, and Memecyloideae (= Memecylaceae DC.). Parsimony and ML yield congruent topologies that place Memecylaceae as sister to Melastomataceae. Pternandra, a Southeast Asian genus of 15 species of which five were sampled, is the first- branching Melastomataceae. This placement has low bootstrap support (72%), but agrees with morphological treatments that placed Pternandra in Melastomatacaeae because of its acrodromal leaf venation, usually ranked as a tribe or subfamily. The interxylary phloem islands found in Memecylaceae and Pternandra, but not most other Melastomataceae, likely evolved in parallel because Pternandra resembles Melastomataceae in its other wood characters. A newly discovered plesiomorphic character in Pternandra, also present in Memecylaceae, is a fibrous anther endothecium. Higher Melastomataceae lack an endothecium as do the closest relatives of Melastomataceae and Memecylaceae. The next deepest split is between Astronieae, with anthers opening by slits, and all remaining Melastomataceae, which have anthers opening by pores. Within the latter, several generic groups, corresponding to traditional tribes, receive solid statistical support, but relationships among them, with one exception, are different from anything predicted on the basis of morphological data. Thus, Miconieae and Merianieae are sister groups, and both are sister to a trichotomy of Bertolonieae, Microlicieae + Melastomeae, and Dissochaeteae + Blakeeae. Sonerileae/Oxysporeae are nested within Dissochaeteae, Rhexieae within Melastomeae, and African and Asian Melastomeae within neotropical Melastomeae. These findings have profound implications for our understanding of melastome morphological evolution (and biogeography), implying, for example, that berries evolved from capsules minimally four times, stamen connectives went from dorsally enlarged to basal/ventrally enlarged, and loss of an endothecium preceded poricidal dehiscence.     

VARIATION IN STRUCTURE AMONG FRUITS OF MALOIDEAE (ROSACEAE)

Fruits of Rosaceae subfamily Maloideae are known as pomes, a fruit type unique to the Maloideae. Using light microscopy we examined the pomes of 173 species, broadly representing the taxonomic diversity of the subfamily. Significant variation occurs among pomes in retention, orientation, and texture of calyx lobes on the distal end of the fruit; density and distribution of sclereids in the flesh; heterogeneity among flesh parenchyma cells; carpel number and number of ovules per carpel; degree of connation among the carpels and adnation between ovary and hypanthium; and texture of the core. Phenetic clustering closely links congeneric fruits. Sorbus is a notable exception; fruits of the compound-leaved species form a cluster unrelated to fruits of the simple-leaved species. Fruits of Malus are also heteromorphic. Division of the Maloideae into two tribes, Crataegeae and Sorbeae, based largely on texture of the core is not substantiated. We hypothesize that the ancestral pome had five carpels, minimal connation of carpels, minimal adnation of ovaries to the hypanthium, two ovules per carpel, and a leathery core. Various adaptations for frugivore dispersal of the seeds partially explain trends in pome evolution.     

Cryptic clades, fruit wall morphology and biology of Andira (Leguminosae: Papilionoideae)

Andira comprises 29 species distributed throughout tropical America, with two subspecies in Africa. Its fruits are unusual for a papilionoid legume because they are drupes. The majority of species have fruits dispersed by bats, but eight species have larger fruits dispersed by-rodents. Some fruits of both dispersal types are secondarily dispersed by water. Cladistic analysis of chloroplast DNA (cpDNA) restriction site characters discovered four well-supported clades of Andira species. None of these 'cryptic' clades had been recognized by previous workers, because they are not apparently marked by any known morphological innovations. This prompted a search for new characters that might support these groupings. An anatomical study of fruit walls of 25 Andira species revealed the presence of three principal endocarp types, dominated by (1) parenchyma, (2) fibres, or (3) stone cells. These features arc best coded as a single unordered multistate character. When incorporated into a simultaneous cladistic analysis of previously gathered molecular and morphological data, states of this endocarp character are shown to be apomorphies for two of the well-supported clades evident in the cpDNA restriction site data. The most likely plesiomorphic state for the endocarp is parenchyma-dominated. Thicker, stronger endocarps of fibres and stone cells may have evolved in response to the need to protect the seed from predators.     

Seed mass and the evolution of fleshy fruits in angiosperms

Fleshy fruits, like drupes and berries, have evolved many times through angiosperm history. Two hypotheses suggest that fleshy fruit evolution is related to changes in the seed mass fitness landscape. The reduced dispersal capability following from an increase in seed mass may be counterbalanced by evolution of traits mediating seed dispersal by animals, such as fleshy fruits. Alternatively, increasing availability and capabilities of frugivores promote evolution of fleshy fruits and allow an increase in seed size. Both these hypotheses predict an association between evolution of fleshy fruits and increasing seed size. We investigated patterns of fruit and seed evolution by contrasting seed mass between fleshy and non‐fleshy fruited sister clades. We found a consistent association between possession of fleshy fruits and heavier seeds. The direction of fruit type change did not alter this pattern; seed mass was higher in clades where fleshy fruits evolved and lower in clades where non‐fleshy fruits evolved, as compared to their sister clades. These patterns are congruent with the predictions from the two hypotheses, but other evidence is needed to distinguish between them. We emphasize the need to integrate studies of seed disperser effectiveness, seed morphology, and plant recruitment success to better understand the frugivores’ role in fleshy fruit evolution.     

Anatomy and development of fruits of Lauraceae from the Middle Eocene Princeton Chert

Investigations of the Middle Eocene Princeton Chert reveal evidence for the connection of lauraceous flowers to fruits through a developmental series. Youngest fruits are found with attached floral remnants. Later stages show receptacle enlargement, fruit wall thickening, and the development of abundant sclereid clusters. Mature fruits are borne on a shallow receptacle and have an endocarp palisade layer of radially elongate cells with stellate outlines, an inner mesocarp layer of radiately arranged sclereid clusters, and a fleshy outer mesocarp layer containing numerous idioblasts with contents. Each mature fruit bears a single seed retaining the outer integument with an innermost radially elongate transfusion cell layer. Mature seeds contain a cellular embryo bearing idioblasts. Fruits are distinguishable from previously described anatomically preserved fossil taxa. This study represents the only documented developmental reconstruction of fossil fruits of Lauraceae and that self-pruning evolved prior to the Eocene. Anatomical modifications over the developmental sequence indicate that different stages of maturity preserved together, may be erroneously identified as several taxa at a fossil locality. Fossil morphotypes typically underestimate species number, but this study suggests that the number of inferred species based on fruit types may be inflated for Lauraceae, potentially exaggerating the tropical interpretation of the paleoenvironment.     

An analysis of diet specialization in frugivorous Pteropus poliocephalus (Megachiroptera) in Australian subtropical rainforest

Abstract The Grey-headed flying fox Pteropus poliocephalus Temminck 1825 is the only mammalian frugivore to occupy substantial areas of the subtropical rainforests of eastern Australia. The composition of the P. poliocephalus diet and diet specialization in the species are therefore pertinent to studies of trophic structure, seed dispersal and evolutionary processes in these forests. During a three-year diet study, P. poliocephalus used fruits from 44 species of canopy and edge plants. Their taxonomically diverse diet was dominated by the Myrtaceae and Moraceae. Dietary specialization by P. poliocephalus was examined using two criteria: the influence of fruit morphology on diet choice and dietary overlap with sympatric avian frugivores. There was no evidence from either approach that they were specialist feeders. Initial analyses comparing the morphological characters of diet fruits with fruits available to P. poliocephalus during the study period showed a preference for white fruits, berries, syconia and fruits with multiple seeds, and avoidance of black fruits and drupes. However, these significant results were not sustained when the confounding effects of correlations between fruit morphology and other traits were considered. All, except the response to berries, could be attributed to either avoidance by P. poliocephalus of secondary compounds in the Lauraceae or selection for the beneficial phenology of Ficus. Dietary overlap with frugivorous birds was notably high and the fruit diet of P. poliocephalus formed a subset of the avian diet. Associations between fruit colour, size and protective mechanisms have been documented in other rainforest areas and have been proposed as indicators of coadaptive relationships between vertebrate frugivores and their diet plants. However, these associations were not apparent in the morphological characters of fleshy fruits from Australian subtropical rainforest trees. An explanatory hypothesis of primarily avian influence on fruit traits is presented.     

Fruit structure of the southern African species of Apodytes Meyer ex Arn. (Icacinaceae)

Fruit development and structure of three southern African species of Apodytes were examined by light and scanning electron microscopy. These are A. dimidiata E. Meyer ex Arn. subsp. dimidiata and two undescribed species designated Apodytes sp. nov. A and B. Fruits are unilaterally developed drupes, ellipsoid and somewhat compressed laterally, with a large succulent appendage. Appendages of A. dimidiata and Apodytes sp. nov. A are predominantly red, whereas those of Apodytes sp. nov. B are a pale translucent green. In all three species the appendages turn black in old fruit. The exocarp is uniseriate and develops solely from the outer epidermis of the ovary wall. The mesocarp is partly parenchymatous, with vascular bundles and cells containing druse crystals of calcium oxalate, and partly lignified (= stone). The uniseriate endocarp s. sir. develops from the inner epidermis of the ovary wall. In a sense the fruit of Apodytes is a composite of parts comparable to a nut (alternatively an achene) and a fleshy drupe. The drupaceous part (fleshy appendage) is a derived structure which develops from the sterile carpel of a reduced locule. We suggest that the fleshy appendage originates as an indicator of seed/fruit maturity, and to attract avian dispersers. Limited field observations support the idea that the red/black appendages of A. dimidiata and Apodytes sp. nov. A also serve as an edible reward for birds. Dispersal of fruit of Apodytes sp. nov. B, with its rather inconspicuously coloured appendage, may be dependent on a specialized fruit/frugivore relationship.     

Characteristics and abundance of vertebrate-dispersed fruits in temperate wet sclerophyll forest in southeastern Australia

The diversity, abundance and display characteristics of plants producing fleshy fruits were recorded in wet sclerophyll forest near Melbourne, Victoria. Fruit characteristics and nutrient content were recorded for 14 species of fruits occurring in the forest and these characteristics compared with similar studies in north temperate and tropical regions. Plants producing fleshy fruits were confined to understorey layers and comprised 13.5% of the native vascular flora. Most species displayed fruits conspicuously by ripening brightly coloured fruits synchronously in large displays. Annual fruit production at three sites ranged from 6.98 to 37.01 kg/ha. Fruit mass, seed number and size were variable but the proportion of pulp per fruit remained remarkably consistent between species. Most fruit pulp contained high quantities of soluble carbohydrates and little lipid or protein. Fruits from wet sclerophyll forest did not differ from fruits from other geographic areas in eight characteristics measured. Although taxonomically distinct, the species in wet sclerophyll forest were not significantly different from other temperate fruits, suggesting that fruit characteristics are under the influence of factors other than phylogeny.     

Tobacco to tomatoes: a phylogenetic perspective on fruit diversity in the Solanaceae

The Solanaceae contains many species of agricultural importance. Several of these are cultivated for their fruits, such as the tomato, the pepper and the aubergine. The family is very diverse in fruit type with capsules, drupes, pyrenes, berries, and several sorts of dehiscent non-capsular fruits occurring in the 90+ genera. In this paper, recent work on fruit type evolution in angiosperms is reviewed in relation to dispersal agents and habitat ecology. Defining fruit types in the Solanaceae in a simple five state system, then mapping them onto a previously published molecular phylogeny based on chloroplast DNA allows discussion of the evolution of these fruit types in a phylogenetic framework. Capsules are plesiomorphic in the family, and although berries are a synapomorphy (shared derived character) for a large clade including the genus Solanum (tomatoes and aubergines), they have arisen several times in the family as a whole. Problems with homology of drupes and pyrenes are discussed, and areas for future investigation of fruit structure homology identified. The distribution of fruit types in the large and diverse genus Solanum is also discussed in the light of monophyletic groups identified using chloroplast gene sequences. This variety is related to recent advances in the understanding of the molecular biology of fruit development. Finally, several key areas of future comparative, phylogenetic investigation into fruit type evolution in the family are highlighted.     

Reproductive ecology of Thymelaea velutina (Thymelaeaceae)- Factors contributing to the maintenance of heterocarpy

Thymelaea velutina (Thymelaeaceae) is a dioecious shrub that presents a unique type of heterocarpy which consists of the simultaneous production of dry and fleshy fruits. It is endemic to the Balearic Islands (Western Mediterranean) and is found both in dunes and mountain areas. The goal of this study was to identify which factors influence the production of both fruit types, examining the variation of their effects at a spatio-temporal scale (comparing two localities in different years). Specifically, we investigated (1) whether pollen limitation influences the type of fruit produced, and (2) the possible differences in seed size, mass, dispersal capacity, seed predation, germination patterns and seedling survival between fruit types. We also examined if the production of fleshy fruits was modified with the application of gibberellins to reproductive branches. Although fleshy fruits were consistently more abundant than dry ones at both populations, their proportion was significantly higher at the site with greater precipitation. The addition of either pollen or gibberellins did not affect the proportion of each fruit type. Seeds in fleshy fruits are consistently larger, heavier and more likely to be dispersed than seeds in dry fruits, but germinability, germination rate and seedling survival was similar among fruit types. Heterocarpy in this species is currently maintained as there is no apparent factor that exerts any strong selective pressure on either fruit type. The two fruit types might even have different `functions', one serving especially for dispersal and population expansion and the other for producing a seed bank that ensures an eventual germination.     

The insect‐focused classification of fruit syndromes in tropical rain forests: An inter‐continental comparison

We propose a new classification of rain forest plants into eight fruit syndromes, based on fruit morphology and other traits relevant to fruit‐feeding insects. This classification is compared with other systems based on plant morphology or traits relevant to vertebrate fruit dispersers. Our syndromes are based on fruits sampled from 1,192 plant species at three Forest Global Earth Observatory plots: Barro Colorado Island (Panama), Khao Chong (Thailand), and Wanang (Papua New Guinea). The three plots differed widely in fruit syndrome composition. Plant species with fleshy, indehiscent fruits containing multiple seeds were important at all three sites. However, in Panama, a high proportion of species had dry fruits, while in New Guinea and Thailand, species with fleshy drupes and thin mesocarps were dominant. Species with dry, winged seeds that do not develop as capsules were important in Thailand, reflecting the local importance of Dipterocarpaceae. These differences can also determine differences among frugivorous insect communities. Fruit syndromes and colors were phylogenetically flexible traits at the scale studied, as only three of the eight seed syndromes, and one of the 10 colors, showed significant phylogenetic clustering at either genus or family levels. Plant phylogeny was, however, the most important factor explaining differences in overall fruit syndrome composition among individual plant families or genera across the three study sites. Abstract in Melanesian is available with online material.     

西藏及其东南地区被子植物与其不同生活型的果实类型分析

统计了分布在西藏自治区的被子植物及各生活型果实的类型及比例,并与藏东南地区做了比较。结果如下,西藏自治区果实以蒴果为主(占37.74%),其次为瘦果、坚果、浆果等;干果的比例远远大于肉果;不同生活型的果实类型谱差异较大,乔木中核果的比例最高,藤本中浆果比例最高,灌木中瘦果比例最高,草本中蒴果占优势;4个生活型中,肉果的比例乔木为最高,其次为藤本、灌木、草本。藏东南地区植物的果实类型也以蒴果为主,其次为瘦果、浆果、核果等;藏东南乔木中核果比例最高,藤本中浆果比例最高,灌木和草本植物以蒴果占优势;乔木肉果的比例最高,其次为藤本、灌木、草本。藏东南肉果比例大于全藏区,而干果比例则相反。果实类型的这些性状特征与各自的环境相适应,是植物长期适应自然环境的进化结果,该研究对于理解植物果实对生态环境的长期适应进化具有一定的意义。     

The ontogeny and structure of the pericarp and seed-coat of Harpephyllum caffrum Bernh. ex Krauss (Anacardiaceae)

The exocarp sensu lato , which develops from the outer epidermis and adjacent parenchyma of the ovary wall, consists of collenchyma cells with a stomatous epidermis. The fleshy, parenchymatous mesocarp or sarcocarp develops after endocarp differentiation. The endocarp is partly spongy and partly woody. The spongy endocarp contains most of the vascular tissue and fills the cavities and grooves of the intricately sculptured outer woody endocarp. The inner woody endocarp and adjacent woody, endocarpal operculum develop from the inner epidermis and subepidermal parenchyma of the ovary wall. The bitegmic, anatropous ovule develops into a derived, exalbuminous seed with an undifferentiated seed-coat. An extensive chalaza, extensive hypostase sensu lato and the raphe are important in the development of the seed-coat. The pericarp and seed-coat of H. caffrum is compared with those of Sclerocarya birrea subsp. caffra and Lannea discolor . The close phylogenetic relationship of these three species of the Spondieae is reaffirmed. The marked similarities in pericarp and seed structure between H. caffrum and species of the genus Spondias are noted.     

The grapevine fleshless berry mutation. A unique genotype to investigate differences between fleshy and nonfleshy fruit

In flowering plants, fruit morphogenesis is a distinct process following fertilization resulting in the formation of a specialized organ associated with seeds. Despite large variations in types and shapes among species, fleshy fruits share common characteristics to promote seed dispersal by animals such as organ growth and metabolite accumulation to attract animal feeding. The molecular biology of fruit ripening has received considerable attention, but little is known about the determinism of early fruit morphogenesis and why some fruits are fleshy while others lack flesh. We have identified in grapevine (Vitis vinifera) a mutation we have named fleshless berry (flb) that reduces by 20 times the weight of the pericarp at ripening without any effect on fertility or seed size and number. The flb mutation strongly impaired division and differentiation of the most vacuolated cells in the inner mesocarp. The timing of ripening was not altered by the mutation although the accumulation of malic acid in the green stage was noticeably reduced while sucrose content (instead of hexoses) increased during ripening. The mutation segregates as a single dominant locus. These results indicate that the Flb- mutant is suitable material to advance our understanding of the genetic and developmental processes involved in the differentiation of an ovary into a fruit.     

Nutritional and Morphological Traits of Invasive and Exotic Fleshy‐fruits in South Africa

While fleshy‐fruited invasive alien plants are recognized as some of the worst invaders on a global scale, until recently, little consideration has been given to the frugivores that feed on these fruits and, more specifically, the fruit traits, which may influence this. We investigated a series of morphological and nutritive fruit traits for ca 30 species of fleshy‐fruited invasive alien and exotic species in South Africa. Invasive alien fruit traits were compared with comparable traits of a similar sample size of indigenous fleshy fruits, which occur in the same area. Finally, the similarity of traits for the same invasive alien species was compared with those fruits in Australia. Invasive alien fleshy fruits were similar in morphology, but greater in some nutritive aspects when compared with indigenous fruits. Furthermore, they were very similar in all aspects to their counterparts in Australia. Most seeds of invasive fleshy fruits were small and light, which may explain some of their invasive success, as benefits associated with small seededness may promote invasive potential. Nutritionally, most invasive alien fleshy‐fruits were hexose‐dominant, containing low lipid and nitrogen content. While frugivore preference trends remain to be formally investigated, this study provides insights into fruit traits, which may tentatively outline why invasive fruits are universally fed on and thus successfully spread.     

Reproductive phenology of Melastomataceae species with contrasting reproductive systems: contemporary and historical drivers

• Flowering and fruiting are key events in the life history of plants, and both are critical to their reproductive success. Besides the role of evolutionary history, plant reproductive phenology is regulated by abiotic factors and shaped by biotic interactions with pollinators and seed dispersers. In Melastomataceae, a dominant Neotropical family, the reproductive systems vary from allogamous with biotic pollination to apomictic, and seed dispersal varies from dry (self‐dispersed) to fleshy (animal‐dispersed) fruits. Such variety in reproductive strategies is likely to affect flowering and fruiting phenologies.
• In this study, we described the reproductive phenology of 81 Melastomataceae species occurring in two biodiversity hotspots: the Atlantic rain forest and the campo rupestre. We aim to disentangle the role of abiotic and biotic factors defining flowering and fruiting times of Melastomataceae species, considering the contrasting breeding and seed dispersal systems, and their evolutionary history.
• In both vegetation types, pollinator‐dependent species had higher flowering seasonality than pollinator‐independent ones. Flowering patterns presented phylogenetic signal regardless of vegetation type. Fruiting of fleshy‐fruited species was seasonal in campo rupestre but not in Atlantic rain forest; the fruiting of dry‐fruited species was also not seasonal in both vegetation types. Fruiting showed a low phylogenetic signal, probably because the influence of environment and dispersal agents on fruiting time is stronger than the phylogenetic affinity.
• Considering these ecophylogenetic patterns, our results indicate that flowering may be shaped by the different reproductive strategies of Melastomataceae lineages, while fruiting patterns may be governed mainly by the seed dispersal strategy and flowering time, with less phylogenetic influence.

     

Evolution of fruit types and seed dispersal:A phylogenetic and ecological snapshot

Success of flowering plants is greatly dependent on effective seed dispersal. Specific fruit types aid different mechanisms of seed dispersal. However, little is known about what evolutionary forces have driven the diversification of fruit types and whether there were phylogenetic constraints on fruit evolution among angio-sperm lineages. To address these questions, we first surveyed the orders and families of angiosperms for fruit types and found no clear association between fruit types and major angiosperm lineages, suggesting there was little phylogenetic constraint on fruit evolution at this level. We then surveyed fruit types found in two contrasting habitats: an open habitat including the Indian desert and North American plains and prairies, and a closed forest habitat of Australian tropical forest. The majority of genera in the survey of tropical forests in Australia were fleshy fruit trees, whereas the majority of genera in the survey of prairies and plains in central North America were herbs with capsules and achenes. Both capsules and achenes are frequently dispersed by wind in the open, arid habitat, whereas fleshy fruits are generally dispersed by animals. Since desert and plains tend to provide continuous wind to aid dispersal and there are more abundant mammal and bird dispersers in the closed forest, this survey suggests that fruit evolution was driven at least in part by dispersal agents abundant in particular habitats.     

果实类型和种子传播的进化:系统发育和生态学简论

Success of flowering plants is greatly dependent on effective seed dispersal. Specific fruit types aid different mechanisms of seed dispersal. However, little is known about what evolutionary forces have driven the diversification of fruit types and whether there were phylogenetic constraints on fruit evolution among angiosperm lineages. To address these questions, we first surveyed the orders and families of angiosperms for fruit types and found no clear association between fruit types and major angiosperm lineages, suggesting there was little phylogenetic constraint on fruit evolution at this level. We then surveyed fruit types found in two contrasting habitats an open habitat including the Indian desert and North American plains and prairies, and a closed forest habitat of Australian tropical forest. The majority of genera in the survey of tropical forests in Australia were fleshy fruit trees, whereas the majority of genera in the survey of prairies and plains in central North America were herbs with capsules and achenes. Both capsules and achenes are frequently dispersed by wind in the open, arid habitat, whereas fleshy fruits are generally dispersed by animals. Since desert and plains tend to provide continuous wind to aid dispersal and there are more abundant mammal and bird dispersers in the closed forest, this survey suggests that fruit evolution was driven at least in part by dispersal agents abundant in particular habitats.     

Fleshy fruits – origins, niche shifts, and diversification

We examined shifts in fruit type, fleshy vs non-fleshy, in relation to habitat-related niche shifts, species richness, and historical distribution, in 50 phylogenetically independent plant lineages. Each lineage consisted of a sister-group pair of fleshy vs non-fleshy taxa and their outgroup. Niche shifts were assessed based on plant community characteristics. Two niche dimensions assumed to reflect community dynamics were derived: spatial predictability of disturbances and canopy closure. Phylogenetically independent origins of fleshy fruit types (1) were correlated with changes to habitats characterized by more shaded and spatially more unpredictable disturbances, (2) had an opposite effect on species richness in woody and herbaceous clades, enhancing species richness in woody clades, and (3) were continuously distributed over a period covering the last 70 million years. These results support the hypothesis that fleshy fruit evolution is driven by vegetation dynamics, and suggest that the strength of frugivore mediated selection on fleshy fruits increases when recruitment sites are spatially unpredictable and/or characterized by low light conditions.