Tânia Wendt

Sympatric bromeliad species (Pitcairnia spp.) facilitate tests of mechanisms involved in species cohesion and reproductive isolation in Neotropical inselbergs

The roles of intra‐ and interspecific gene flow in speciation and species evolution are topics of great current interest in molecular ecology and evolutionary biology. Recent modelling studies call for new empirical data to test hypotheses arising from the recent shift from a ‘whole‐genome reproductive isolation’ view to a ‘genic’ view of species and speciation. Particularly scarce (and thus of particular interest) are molecular genetic data on recently radiated, naturally hybridizing species in strongly structured and species‐rich environments. Here, we studied four sympatric plant species (Pitcairnia spp.; Bromeliaceae) adapted to Neotropical inselbergs (isolated outcrops resembling habitat ‘islands’ in tropical rainforests) using nuclear and plastid DNA. Patterns of plastid DNA haplotype sharing and nuclear genomic admixture suggest the presence of both, incomplete lineage sorting and interspecific gene flow over extended periods of time. Integrity and cohesion of inselberg species of Pitcairnia are maintained despite introgression and in the face of extremely low within‐species migration rates (Nem < 1 migrant per generation). Cross‐evaluation of our genetic data against published pollination experiments indicate that species integrity is maintained by the simultaneous action of multiple prezygotic barriers, including flowering phenology, pollinator isolation and divergent mating systems. Postzygotic Bateson–Dobzhansky–Muller incompatibilities appear to contribute to isolation, as suggested by asymmetric introgression rates of single loci. Our results suggest that incomplete lineage sorting, hybridization and introgression form integral aspects of adaptive radiation in Neotropical inselberg ‘archipelagos’. Inselbergs with multiple closely related co‐occurring species should be of special interest to students of speciation in mountain systems, and to ongoing conservation programmes in the Atlantic Rainforest biodiversity hotspot.

Selfing facilitates reproductive isolation among three sympatric species of Pitcairnia (Bromeliaceae)

Abstract. The reproductive biology of three sympatric species Pitcairniaflammea, P. corcovadensis and P. albiflos (Bromeliaceae) was studied on Corcovado Mountain in the city of Rio de Janeiro, Brazil. Controlled pollination experiments were also conducted using plants transplanted to a greenhouse. The three species are self-compatible and interspecifically cross compatible. Pitcairnia corcovadensis was principally an autonomous self-pollinator, having scarce pollinator activity, anthers and stigmas at the same level, and absence of nectar. In P. flammea, many flowers opened per day, the stigma and anther were close to each other, and its nectar was regularly consumed by hummingbirds; all factors that promote geitonogamy in this species. Although fully self-compatible, P. albiflos always opened a few flowers per days showing an adaptation to cross-pollination. Observations during two flowering seasons showed that despite different times for peak flowering, blooming of these three species overlapped in April. They grow in mixed clumps that may facilitate promiscuous pollination between them but no intermediate forms were observed under natural conditions. The absence of temporal isolation, geographic isolation and isolation via post-pollination reproduction suggests that evolution toward selfing was important to avoid hybridization between these sympatric species.

Breeding systems of Bromeliaceae species: evolution of selfing in the context of sympatric occurrence

Co-occurring congener plant species in the highly diverse Atlantic forests of southeastern Brazil may act as natural laboratories for evaluating evolution of reproductive shifts. We assessed the breeding systems in a sympatric assemblage of bromeliad species and compiled literature available for the family to compare our experiments with available information. We performed controlled experiments of autonomous selfing, self- and cross-pollination in 40 species of 11 genera of two subfamilies that, in general, overlap their blooming period and share the same pollination vectors. We also tested for differences between self-compatible (SC) and self-incompatible (SI) species with regard to ecological factors such as abundance, co-flowering and co-occurrence. Most species experimentally tested and surveyed in the literature (75%) were SC. Species from the subfamily Tillandsioideae were predominantly SC, while Bromelioideae showed greater variation in breeding systems. About 43% of the species studied set fruits spontaneously in the absence of pollinator vectors. We found that SC species were the more abundant, were more frequently associated with other relatives and overlapped their blooming period with other species more than SI species. Thus, our results suggest that self-compatibility is common for Bromeliaceae and do not support the traditional hypothesis of reproductive assurance used to explain the evolution of selfing. We discuss self-compatibility as a reproductive isolating mechanism in the presence of pollen flow among sympatric congener species.

High abundance of dioecious plants in a tropical coastal vegetation

We examined the frequency of hermaphroditic, monoecious, and dioecious species of angiosperms in restinga (sandy coastal plain) vegetation in SE Brazil. The study site was a vegetation mosaic comprising nine plant formations, ranging from open types to forest. Dioecy (14% of 566 species) was similar to other tropical vegetations and strongly associated with woodiness and entomophily. However, more interestingly, there was an exceptionally high percentage (35%) of dioecious species among the dominant woody plants. This pattern has not been previously reported, and we discuss the extent to which it is ecologically driven. We argue that the high abundance of dioecious plants in this resource-poor environment can be attributed to ecological traits related to long-distance dispersal, ecological vigor, and possibly, vegetative reproduction.

An apparent lack of prezygotic reproductive isolation among 42 sympatric species of Bromeliaceae in southeastern Brazil

The Atlantic rainforest in southeastern Brazil is one the main centers of diversification of Bromeliaceae. Empirical estimates of the relative importance of different pre- and postzygotic barriers to gene flow between recently diverged species are important for understanding speciation processes. While many bromeliad species easily hybridize in cultivation, few records of natural hybrids between closely related sympatric species suggest the existence of strong prezygotic barriers. A community of 42 sympatric bromeliad species, represented by nine genera (Aechmea, Billbergia, Edmundoa, Neoregelia, Nidularium, Quesnelia, Racinaea, Tillandsia, and Vriesea), were surveyed from 2004–2005 to assess the role of microhabitat isolation, phenological isolation and ethological isolation as potential prezygotic barriers. These bromeliads are abundant in the understory and frequently grow densely aggregated in multispecific patches that may facilitate promiscuous pollination. There was a large overlap of flowering periods even between congeneric species. Most species shared a similar assemblage of flower visitors; the hummingbird Rhamphodon naevius was the major visitor for 35 species. Only one putative hybrid was observed. This uncommonness of hybridization is puzzling, given that the prezygotic isolation mechanisms investigated are potentially weak to effectively avoid interspecific pollination.

Monophyly and Phylogenetic Relationships in Lymania (Bromeliaceae: Bromelioideae) Based on Morphology and Chloroplast DNA Sequences

Abstract A cladistic analysis of Lymania was conducted using morphology and sequences from three chloroplast DNA regions: the matK coding region and the psbA-trnH and trnL-trnF intergenic spacers. The monophyly of the genus and the phylogenetic relationships among related genera were examined. Of the nine Lymania species, eight are endemic to southern Bahia, Brazil. Lymania is the first genus in Bromeliaceae subfamily Bromelioideae to be subjected to a combined morphological and molecular analysis. The genera of Bromelioideae have been particularly difficult to classify and there has been disagreement about their interrelationships and monophyly. Morphological data show better resolution than molecular data alone. The partition homogeneity test supported a combined analysis of the two data sets, yielding a single most parsimonious tree. In the combined analysis, monophyly of Lymania is moderately supported, and the genus is closely related to species of Aechmea subg. Lamprococcus and subg. subg. Ortigiesia. The morphological distinctiveness coupled with low molecular divergence indicates relatively recent and rapid speciation within Lymania. The combined analysis of morphological and molecular data as done in this study provides a framework for future research on other Bromelioideae genera that could foster better taxonomic rearrangements.

Recognition of Pitcairnia corcovadensis (Bromeliaceae) at the Species Level

Abstract Pitcairnia flammea var. corcovadensis was formed by the reduction of P. corcovadensis. The re-establishment of the latter taxon is based on two points: (1) P. corcovadensis occurs sympatrically with P. flammea in many locations, and (2) a morphometric analysis on a natural population involving these two taxa showed that they were distinct and no intermediate form was found despite their overlapping flowering seasons. Herbarium collections were examined to verify that this distinction is consistent throughout their geographic distribution. Despite the apparent reproductive isolation, artificial hybrids can be produced between P. corcovadensis, and P. flammea. Five morphological traits were recorded for 221 six-month old seedlings from artificial hybrids and parental taxa that were grown under the same controlled conditions. Analysis of variance and discriminant analysis on seedlings showed the differences to be genetically based. A brief review of the synonyms related to P. flammea complex concluded that P. lancifolia var. lancifolia, P. lancifolia var. minor, and P. pumila are synonyms of P. corcovadensis. A re-description, an epitype establishment, geographic distribution, description and list of material examined are provided for P. corcovadensis. Communicating Editor: Paul Wilson

Mating system variation and assortative mating of sympatric bromeliads (Pitcairnia spp.) endemic to neotropical inselbergs

PREMISE OF THE STUDY The mating system is an important component of the complex set of reproductive isolation barriers causing plant speciation. However, empirical evidence showing that the mating system may promote reproductive isolation in co-occurring species is limited. The mechanisms by which the mating system can act as a reproductive isolation barrier are also largely unknown. METHODS Here we studied progeny arrays genotyped with microsatellites and patterns of stigma-anther separation (herkogamy) to understand the role of mating system shifts in promoting reproductive isolation between two hybridizing taxa with porous genomes, Pitcairnia albiflos and P. staminea (Bromeliaceae). KEY RESULTS In P. staminea, we detected increased selfing and reduced herkogamy in one sympatric relative to two allopatric populations, consistent with mating system shifts in sympatry acting to maintain the species integrity of P. staminea when in contact with P. albiflos. CONCLUSIONS Mating system variation is a result of several factors acting simultaneously in these populations. We report mating system shifts as one possible reproductive barrier between these species, acting in addition to numerous other prezygotic (i.e., flower phenology and pollination syndromes) and postzygotic barriers (Bateson-Dobzhansky-Muller genetic incompatibilities).

Leaf anatomy and its contribution to the systematics of Aechmea subgenus Macrochordion (de Vriese) Baker (Bromeliaceae)

The leaf anatomy of the species Aechmea subgenus Macrochordion was analyzed to obtain valuable data on their taxonomic delimitation and to identify anatomical adaptations to their respective habitats and habits. All leaves of these species are hypostomatic, and present: peltate trichomes on both surfaces; stomata sunk in epidermal depressions; small epidermal cells with thick walls and inclusions of silica bodies; a mechanical hypodermis; an aquiferous parenchyma; chlorenchyma with fibrous clusters and air channels; and vascular bundles surrounded by a parenchymatic sheath and a cap of fibers. The results are evaluated within an adaptive and taxonomic context. Variations in hypodermic thickening, amount of water parenchyma, position of the air channels and shape of the cells filling the air channels are useful for delimiting groups of species, strengthening the relationships suggested by their external morphology.

Natural hybridization and genetic and morphological variation between two epiphytic bromeliads

We investigated the potential evolutionary mechanisms associated with maintenance of reproductive species barriers between V. simplex and V. scalaris through morphological and genetic data. Nuclear genomic admixture suggests hybridization in sympatric populations, although interspecific gene flow is low among species in all sympatric zones (N < 0.5). Thus, morphological and genetic divergence (10.99%) between species can be maintained despite ongoing natural hybridization. Cross-evaluation of our genetic and morphological data suggests that species integrity is maintained by the simultaneous action of multiple barriers, such as divergent reproductive systems among species and differences in floral traits.