ABSTRACT Distyly is a floral polymorphism with reciprocal placement of male and female structures, heteromorphic self-incompatibility, and other ancillary traits. However, breeding system breakdowns and loss of polymorphism are common. Here we traced the diversification of breeding strategies in the type genera of tribes Palicoureeae and Psychotrieae and discussed the evolution of distyly in a phylogenetic framework. We used literature and field information for breeding systems transitions in 46 species of Palicourea and Psychotria. Beyond distyly, we found four additional breeding systems, including monomorphism with herkogamy, homostyly (without herkogamy), monoecy and dioecy. Breeding transitions arose independently and were mostly derived from distyly. Only two species presented monomorphism as an intermediate state into gender specialization. It was not possible to evaluate the origin and evolutionary pathways for distyly in Psychotria and Palicourea as a whole, since distyly seems to be ancestral to their diversification. Breeding transitions in Psychotria and Palicourea appeared to be phylogenetically and biogeographically independent and occurred mostly in islands or isolated forest fragments, with distinct divergence times. Breeding transitions were not related to changes in ploidy. We propose that evolution of breeding transitions in Psychotria and Palicourea represent phylogenetically independent strategies to reproductive assurance in isolated or disturbed habitats.

Resumo A heterostilia é um polimorfismo floral geneticamente controlado onde populações de plantas apresentam dois ou três morfos com peças reprodutivas em alturas recíprocas entre os morfos. Em populações naturais, espera-se encontrar uma razão igual entre os morfos (isopletia). O objetivo do estudo foi caracterizar o sistema reprodutivo, a biologia floral, as características heterostílicas, incluindo reciprocidade das peças reprodutivas, fenologia e polinização em Palicourea crocea, uma espécie arbustiva do sub bosque de formações florestais do Cerrado. Para tal foram medidas estruturas florais, realizados cruzamentos controlados, observados os visitantes florais, além de acompanhamento fenológico. Palicourea crocea é uma espécie distílica típica, autoincompatível, com altos índices de hercogamia recíproca entre os morfos. Polinizada preferencialmente por beija-flores, além de mariposas e abelhas. Houve formação maior de frutos em polinização cruzada intermorfo (> 50%) e menor formação em polinização intramorfo (< 20%) e autopolinização (< 13%). Esses dados foram confirmados pelo não crescimento de tubos polínicos em pistilos autopolinizados e polinizados de forma intramorfo. A floração é anual, e ocorre entre os meses de novembro e fevereiro, com pico de floração em dezembro e janeiro. Os dados reprodutivos avaliados se mostram similares a outras espécies de Rubiaceae do sub bosque de ambientes florestais do Cerrado.

Abstract The heterostyly is a floral polimorphysm genetically controlled where populations of plants present two or three morphs with reproductive structures in reciprocal heights among the morphs. In natural populations, a balanced ratio between morphs (isoplethy) is expected. The objective of the study was to characterize the breeding system, the floral biology, the characteristics of heterostyly, including reciprocity of reproductive parts, the phenology and pollination in Palicourea crocea, a shrub species of the understory of forest formations of Cerrado. For such measures were floral structures, held controlled crossings, observed flower visitors, in addition to phenological monitoring. Palicourea crocea is proved to be a typical distylous species, self-incompatible, with high levels of reciprocal herkogamy between the morphs. Preferentially pollinated by hummingbirds, followed by moths and bees. There was a higher fruit formation in cross-pollination intermorph (> 50%) and lower fruit formation intramorph pollination (< 20%), and self-pollination (< 13%). These data were confirmed by the not growth of pollen tubes in self-pollination and pollinated intramorph pistils. Flowering is annual and occurs between the months of November and February, with peak flowering in December and January. Reproductive data evaluated to show similar to other species of Rubiaceae of the understory of forest formations of Cerrado.

ABSTRACT Angiosperms display an enormous diversity of forms, functions and strategies when it comes to reproduction. This multiplicity has been translated into several terminological concepts and contexts, which have facilitated further research. On the other hand, the use of terms that address the reproduction of flowering plants has been shown to be inconsistent in the literature, complicating communication among specialists. Key terms, such as “reproductive system”, “mating system” and “sexual system”, among others, have been frequently cited as synonyms, and even used in different circumstances. This review proposes to establish a consistent nomenclatural classification in the field of angiosperms reproductive biology in order to facilitate communication among researchers. Specific terms related to angiosperm reproduction are conceptualized and distributed into five general systems: four related to sexual reproduction (sexual, floral, incompatibility and mating systems); and one related to asexual reproduction (apomictic systems). Our proposal is not to establish a natural classification, but rather to provide a general overview of the main concepts that were grouped here in an artificial and functional manner. Our aim is to advance the field of reproductive biology of angiosperms with consistent and well-defined applications of relevant terminologies.

RESUMO Apresentamos listagem da entomofauna visitante de flores do estado de Mato Grosso do Sul (MS) com base na compilação de informações obtidas em 17 estudos, a maioria realizado em áreas de Cerrado (n = 11) e menos frequentemente no Pantanal (n = 6). Foram registrados 10 grupos de insetos, pertencentes a seis ordens, 80 famílias e 411 espécies. Maior riqueza foi amostrada para o Cerrado (307 spp.) que Pantanal (147 spp.), com somente 43 espécies (10,4%) em comum entre estes biomas. Anthophila foi o grupo mais rico (155 spp.), seguido por besouros (82), borboletas/mariposas (53) e vespas (45), que junto totalizaram 81,5% das espécies. Maior riqueza de abelhas está relacionada ao fato da maioria dos trabalhos enfocarem este grupo, além da especialização deste grupo na utilização de recursos florais. Surpreendente foi o segundo lugar ocupado por besouros em relação a outros visitantes mais “ativos” e “habituais”, como lepidópteros e moscas. Em MS os acervos e grupos de pesquisa com entomofauna antófila são restritos e/ou incipientes, sendo necessário fortalecimento dos mesmos através de parcerias, intercâmbios e formação de recursos humanos na área.

ABSTRACT We present a checklist of the anthophilous entomofauna of Mato Grosso do Sul state (MS) based on information compiled from 17 studies, most of them achieved in Cerrado vegetation (n = 11) and less frequently in the Pantanal (n = 6). We recorded 10 groups of insects, belonging to six orders, 80 families and 411 species. Higher richness was sampled for Cerrado (307 spp.) compared to Pantanal (147 spp.), with only 43 species (10.4%) common to both biomes. Anthophila was the richest group (155 spp.), followed by beetles (82), butterflies/moths (53) and wasps (45), which totalized 81.5% of species. The highest richness of bees is related to the fact the most studies are concentrated in this group, besides the specialization of this group in utilization of floral resources. Surprising was the beetles occupying second place compared to others more “active” and “habitual” visitors, such as butterflies and flies. The entomofauna collections and research teams in MS are limited and/or incipient and they should be strenghtened through partnerships, exchange and capacity building in this biological group.

Resumo Espécies distílicas possuem populações com dois morfos florais. O morfo longistilo possui flores com pistilos longos e estames curtos e o morfo brevistilo, pistilos curtos e estames longos. Normalmente, os morfos apresentam um sistema heteromórfico de incompatibilidade e os morfos estão em uma razão de 1:1 (isopletia) nas populações. Diferentes variações podem ser encontradas em espécies distílicas, como a presença de autocompatibilidade, anisopletia e variações no nível de reciprocidade entre anteras e estigmas dos dois morfos. O objetivo desse trabalho foi investigar a ocorrência das características distílicas em duas espécies de Rubiaceae. Para isso, a razão dos morfos, a hercogamia recíproca, o sistema de incompatibilidade e os visitantes florais de Psychotria deflexa e Declieuxia fruticosa foram estudados. Ambas as espécies apresentaram os dois morfos em proporção semelhante, altos valores de reciprocidade entre a altura dos verticilos sexuais dos morfos florais e apenas insetos como visitantes florais. O morfo brevistilo das duas espécies apresentou autoincompatibilidade parcial. Dentro de Rubiaceae, mesmo em grupos filogenéticos distintos, o relaxamento ou quebra da distilia parece ocorrer em padrões similares e comumente tal variação é mais comum no morfo longistilo. Para as espécies estudadas, mesmo com a pseudocompatibilidade do morfo brevistilo, as populações apresentaram proporção igual dos morfos, indicando que fatores como a alta hercogamia recíproca e, possivelmente, o serviço de polinização podem promover a manutenção da isopletia característica da distilia.

Abstract Distylous species have populations with two floral morphs. The pin morph has long pistils and short stamens while the thrum morph presents short pistils and long stamens. Usually heterostylous plants present a diallelic system of incompatibility and morphs occur in a 1:1 ratio (isoplethy) in the populations. Different forms of variations occur in distylous species, such as the presence of self-compatibility, anisoplethy and variation in the reciprocity level between anthers and stigmas of the two floral morphs. The aim of this study was to investigate the occurrence of the distylous characteristics in two Rubiaceae species. For this purpose, morph ratio, reciprocal herkogamy, incompatibility system and flower visitors of Psychotria deflexa and Declieuxia fruticosa were studied. Both species have the two floral morphs in equal ratio, high reciprocity values for height of the reproductive whorls of the floral morphs and were visited only by insects. However, the thrum morph on both species presented partial self-incompatibility. Within the Rubiaceae, even in distinct phylogenetic groups, weakening or breakdown of distyly seems to occur in similar patterns, but deviations in the incompatibility system have been mostly recorded for the pin morph of distylous species. In the studied species the populations had equal morph ratio despite the pseudocompatibility of the thrum morph, which indicates that factors such as high reciprocal herkogamy and possibly efficient pollination services could promote the maintenance of distyly in these species.

Distyly is a genetically controlled floral dimorphism, characterized by the reciprocal positioning of pin and thrum morphs, a heteromorphic incompatibility system and a balanced morph ratio (isoplethy). This study aimed to investigate the phenology, features of distyly, reproductive biology, and floral visitors of Psychotria goyazensis Mull. Arg. (Rubiaceae), an intramorph self-compatible species, in a tropical semideciduous forest in the municipality of Catalão, located in the state of Goiás, Brazil. The phenology was recorded for a sample of individuals, the floral morphology being described using fresh and fixed material. The incompatibility system was tested using controlled hand pollinations. Floral visitors were collected and identified. Blooming began in November 2009 and ended in April 2010. Fruits developed from December 2009 to March 2010. The population presented atypical distyly, because only plants with pin flowers were found. The intramorph and open pollinations set more fruits than did spontaneous self-pollinations. The main flower visitors were Systropus sp. (Diptera), as well as Hymenoptera and Lepidoptera species. Morphological variations in distyly can occur by breakdown/permutation of the gene that controls the polymorphism. However, some authors argue that, in Rubiaceae, genetic control of the incompatibility system can operate independently of the morphological factor, and species might respond in different ways to the same selective pressures.

Structural differences between cerrado species with different leaf phenologies are linked to crown architecture, leaf production, and biomass allocation to shoots and leaves. The present study characterized crown structures and the patterns of biomass allocation to leaves and shoots in two woody cerrado species with contrasting leaf phenologies and quantified the irradiance reaching their leaves to determine the best period during the day for photosynthetic activity. The shoots and leaves of five individuals of both Annona coriacea (deciduous) and Hymenaea stigonocarpa (evergreen) were collected along a 50 m transect in a cerrado fragment within the urban perimeter of Catalão - GO, to determine their patterns of biomass allocation in their crowns. The evergreen H. stigonocarpa had significantly higher mean values of shoot inclination (SI), petiole length (PL), leaf area (LA), leaf display index (LDI), and individual leaf area per shoot (ILA), while the deciduous species A. coriacea had significantly higher leaf numbers (LN). The more complex crown of H. stigonocarpa had shoots in more erect positions (orthotropic), with intense self-shading within shoots; A. coriacea, on the other hand, had slanting (plagiotropic) shoots in the crown, allowing similar irradiance levels to all leaf surfaces. The production of plagiotropic shoots by the deciduous species (A. coriacea) is a strategy that enables its use of incident sunlight early in the morning and preventing excessive water loss or excessive irradiance. Hymenaea stigonocarpa (an evergreen), by contrast, had orthotropic shoots and uses intense self-shading as a strategy to avoid excessive irradiance, especially at midday. Differences in crown architectures between evergreen and deciduous species of cerrado sensu stricto can therefore be viewed as adaptations to the environmental light regime.

Distilia é um tipo de sistema reprodutivo que utiliza características morfológicas e fisiológicas como forma de potencializar a xenogamia. Dentre as 25 famílias de Angiospermas que apresentam esse sistema, Rubiaceae é a que tem a maior riqueza. Este estudo teve como objetivo investigar os aspectos relacionados ao sistema distílico de quatro espécies de Palicourea distribuídas no Cerrado do Brasil Central: Palicourea marcgravii A. St.-Hil., P. officinalis Mart., P. coriacea (Cham.) K. Schum. e P. macrobotrys (Ruiz & Pav.) Roem. & Schult. As áreas de coleta no Distrito Federal foram: Parque Nacional de Brasília, Estação Ecológica de Águas Emendadas e Reseva Ecológica do IBGE. As espécies Palicourea marcgravii e P. officinalis apresentaram-se como distílicas em função da presença dos dois morfos florais, da sua razão equilibrada e do sistema de incompatibilidade auto e intramorfo. As espécies P. coriacea e P. macrobotrys apresentaram-se como variantes pela ocorrência de indivíduos com morfo homostilo, além da distilia na primeira espécie e pelo morfo homostilo ser dominante na segunda espécie. Não se sabe ainda as forças evolutivas que determinam essas variações, contudo acredita-se que as características genéticas intrínsecas de cada táxon têm uma considerável influência e que cada espécie pode responder de forma diferente, ou até mesmo não responder, perante as mesmas pressões seletivas a que estão submetidas.

Distyly is a type of reproductive system whose morphological and physiological features are used as a mechanism for increasing the xenogamy. Among the 25 Angiosperm families presenting this system, Rubiaceae is the richest. The objective of this study was to characterize the distylous system of four Palicourea species from the Cerrado of Central Brazil, Palicourea marcgravii A. St.-Hil., P. officinalis Mart., P. coriacea (Cham.) K. Schum. e P. macrobotrys (Ruiz & Pav.) Roem. & Schult. This study took place in the following areas of Distrito Federal: Parque Nacional de Brasília, Estação Ecológica de Águas Emendadas e Reseva Ecológica do IBGE. The species Palicourea marcgravii and P. officinalis were typicall distylous due to the presence of two floral morphs, the in ratio, and also the self and intramorph incompatibility. However, P. coriacea and P. macrobotrys species were variants because homostylous individuals occur together with distylous morphs in first specie, and because the homostyle morph is dominant in the second. It is still unknown which evolutional drivers determine those differences. However, it is likely that intrinsic genetics characteristics of each taxon have a considerable influence, and also that species may respond differently to the same selective pressures, or they may not present any response.

A heterostilia é um polimorfismo floral geralmente associado a sistemas genéticos de intramorfo incompatibilidade. Nós avaliamos aspectos reprodutivos da heterostilia de uma população de Rourea induta Planch. em uma área de cerrado de Brasília, DF. Foram conduzidos estudos sobre sua biologia floral, sistema reprodutivo, produção e maturação de frutos, germinação de sementes, fenologia reprodutiva e visitantes florais. As flores são pequenas (11 mm de diâmetro), com morfologia simples e possuem dois grupos de cinco estames de comprimentos diferentes e cinco pistilos. O comprimento médio de estames e pistilos diferiu significativamente entre o morfo brevistilo e o longistilo. No entanto, não houve hercogamia recíproca completa entre os dois morfos florais. Os dois morfos são intramorfo incompatíveis, mas o morfo brevistilo é completamente auto-incompatível enquanto o longistilo é parcialmente autocompatível. Apesar das diferenças na morfologia floral e no sistema reprodutivo entre os morfos, estes apresentam igual sucesso reprodutivo em condições naturais, uma vez que a produção e a maturação de frutos por planta e a taxa de germinação das sementes não diferiram significativamente. A população de R. induta apresentou floração tipo "pulsed bang" com alta sincronia intra-individual e inter-individual de floração. Grande variedade de insetos, principalmente pequenas abelhas sociais, foi observada visitando as flores. Nossos resultados sugerem que a auto-incompatibilidade parcial, a incompatibilidade intramorfo e as diferenças nas alturas dos verticilos reprodutivos entre os dois morfos reduzem os níveis de autogamia em R. induta. Em última análise, a maior produção de frutos por polinização intermorfo, promoveu a razão isoplética na população estudada e indicou que R. induta é dependente dos polinizadores para a reprodução sexuada.

Heterostyly is a floral polymorphism usually associated to intramorph-incompatible mating system. We evaluated reproductive aspects of heterostyly in a Rourea induta Planch. population in a cerrado area of Brasília, Central Brazil. Analyses of the floral biology, breeding systems, fruit set and maturation, seed germination, reproductive phenology and floral visitors of were conducted. The flowers are small (about 11 mm diameter), with single morphology, and have five pistils and two sets of five stamens of unequal lengths. The average lengths of stamens and pistils were significantly different between thrum and pin morphs. However, complete reciprocal herkogamy was not found between stamen and pistil lengths of the two floral morphs. Both morphs are intramorph-incompatible. However, thrums are completely self-incompatible while pins are partially self-compatible. In spite of the differences in the floral morphology and breeding system, the two morphs had similar reproductive success in natural condition. The two floral morphs did not differ significantly in terms of fruit setting and maturation or seed germination rate. Rourea induta produced abundant flowers daily over two short events ("pulsed bang" flowering) and most plants in the population flowered synchronously. Many species of insects, mainly small social bees, were observed visiting the flowers. Our results suggest that partial self-incompatibility, intramorph-incompatibility, and differences between morphs in lengths of stamens and pistils reduced autogamy levels in R. induta. Ultimately, the higher fruit setting by intermorph pollination promotes isoplety and indicates that sexual reproduction in R. induta population depends on pollinators services.

Rubiaceae é a maior família que contém espécies distílicas dentre as Angiospermas. A distilia nessas espécies pode apresentar variações de diferentes formas e graus, originando derivações como homostilia, monomorfia e dioicia. Este estudo tem objetivo de descrever a biologia floral, a polinização e o sistema reprodutivo de Manettia cordifolia Mart. O estudo foi realizado na Estação Ecológica do Panga e margens do Rio Uberabinha (Uberlândia, MG) e complementado com observações de material botânico depositado em herbários. Manettia cordifolia é uma liana com flores tipicamente ornitóflias. Seu polinizador principal foi o beija-flor Phaetornis pretrei. A espécie não foi considerada distílica, apesar de estar dentro de gênero considerado distílico. Suas características indicam ocorrência de monomorfismo longistílico, provavelmente derivado de um ancestral distílico, não sendo encontrados indivíduos brevistilos. Os testes de polinizações controladas indicam que a espécie é auto-incompatível e não apomítica. O crescimento do tubo polínico até o ovário após autopolinização é similar ao observado em flores longistilas de espécies verdadeiramente distílicas. A interpretação dos resultados é dificultada pela ausência de informações sobre o controle genético da heterostilia nas Rubiaceae.

Rubiaceae is the largest family with distylous species among the Angiosperms. The distyly in those species may vary in form and degree leading to homostyly, monomorphism and dioecy. The objective of this study was to describe the floral biology, pollination and breeding system of Manettia cordifolia Mart. The study was carried out in The Panga Ecological Station and riverside of the Uberabinha (Uberlândia, MG), and complemented with observations of collections deposited in herbaria. Manettia cordifolia is a vine with flower traits of typical of hummingbird pollination syndrome. The main pollinator was the hummingbird Phaetornis pretrei. The plant cannot be considered a distylous species, although it is in a genera known as distylous. The observed characteristics indicate a species with pin-monomorphy, probably derived from a distylous ancestral. Controlled pollinations showed a self-incompatible and non-apomictic species. Pollen tube growth down to the ovary after selfing is similar to the observed in pin pistils of truly distylous congeneric species. The absence of information on the distyly genetic control in the Rubiaceae makes it difficult to interpret the variations observed on the present study.