[Show abstract][Hide abstract] ABSTRACT: Symbioses include some of the clearest cases of coevolution, but their origin, loss or reassembly with different partners can rarely be inferred. Here we use ant/plant symbioses involving three plant clades to investigate the evolution of symbioses. We generated phylogenies for the big-eyed arboreal ants (Pseudomyrmecinae), including 72% of their 286 species, as well as for five of their plant host groups, in each case sampling more than 61% of the species. We show that the ant-housing Vachellia (Mimosoideae) clade and its ants co-diversified for the past 5 Ma, with some species additionally colonized by younger plant-nesting ant species, some parasitic. An apparent co-radiation of ants and Tachigali (Caesalpinioideae) was followed by waves of colonization by the same ant clade, and subsequent occupation by a younger ant group. Wide crown and stem age differences between the ant-housing genus Triplaris (Polygonaceae) and its obligate ant inhabitants, and stochastic trait mapping, indicate that its domatium evolved earlier than the ants now occupying it, suggesting previous symbioses that dissolved. Parasitic ant species evolved from generalists, not from mutualists, and are younger than the mutualistic systems they parasitize. Our study illuminates the macroevolutionary assembly of ant/plant symbioses, which has been highly dynamic, even in very specialized systems.
Proceedings of the Royal Society B: Biological Sciences 12/2015; 282(1819). DOI:10.1098/rspb.2015.2200 · 5.05 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Experimental data on the perception of day length and temperature in dormant temperate zone trees are surprisingly scarce.
In order to investigate when and where these environmental signals are perceived, we carried out bagging experiments in which buds on branches of Fagus sylvatica, Aesculus hippocastanum and Picea abies trees were exposed to natural light increase or kept at constant 8-h days from December until June. Parallel experiments used twigs cut from the same trees, harvesting treated and control twigs seven times and then exposing them to 8- or 16-h days in a glasshouse.
Under 8-h days, budburst in Fagus outdoors was delayed by 41 d and in Aesculus by 4 d; in Picea, day length had no effect. Buds on nearby branches reacted autonomously, and leaf primordia only reacted to light cues in late dormancy after accumulating warm days. Experiments applying different wavelength spectra and high-resolution spectrometry to buds indicate a phytochrome-mediated photoperiod control.
By demonstrating local photoperiodic control of buds, revealing the time when these signals are perceived, and showing the interplay between photoperiod and chilling, this study contributes to improved modelling of the impact of climate warming on photosensitive species.
New Phytologist 06/2015; DOI:10.1111/nph.13510 · 7.67 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: It is plausible that specialized ecological interactions constrain geographic ranges. We address this question in neotropical bees, Centris and Epicharis, that collect oils from flowers of Calceolariaceae, Iridaceae, Krameriaceae, Malpighiaceae, Plantaginaceae, or Solanaceae, with different species exploiting between one and five of these families, which either have epithelial oil glands or hair fields. We plotted the level of oil-host specialization on a clock-dated phylogeny for 22 of the 35 species of Epicharis and 72 of the 230 species of Centris (genera that are not sister genera) and calculated geographic ranges (km(2) ) for 23 bee species based on collection data from museum specimens. Of the oil-offering plants, the Malpighiaceae date to the Upper Cretaceous, while the other five families are progressively younger. The stem and crown groups of the two bee genera date to the Cretaceous, Eocene, and Oligocene. Shifts between oil hosts from different families are common in Centris, but absent in Epicharis, and the direction is from flowers with epithelial oil glands to flowers with oil hairs, canalized by bees' oil-collecting apparatuses, suitable for piercing epithelia or mopping oil from hair fields. With the current data, a link between host specialization and geographic range size could not be detected. This article is protected by copyright. All rights reserved.
This article is protected by copyright. All rights reserved.
[Show abstract][Hide abstract] ABSTRACT: The 361 species of hummingbirds that occur from Alaska to Patagonia pollinate ~7,000 plant species with flowers morphologically adapted to them. To better understand this asymmetric diversity build-up, this study analyzes the origin of hummingbird/plant mutualisms in North America and temperate South America, based on new compilations of the 184 hummingbird-adapted species in North America, the 56 in temperate South America, and complete species-level phylogenies for the relevant hummingbirds in both regions, namely five in temperate South America and eight in North America. Because both floras are relatively well sampled phylogenetically, crown or stem ages of many representative clades could be inferred. The hummingbird chronogram was calibrated once with fossils, once with substitutions rates, while plant chronograms were taken from the literature or in 13 cases newly generated.
The 184 North American hummingbird-adapted species belong to ca. 70 lineages for 19 of which (comprising 54 species) we inferred divergence times. The 56 temperate South American hummingbird-adapted species belong to ca. 35 lineages, for 17 of which (comprising 25 species) we inferred divergence times. The oldest hummingbirds and hummingbird-adapted plant lineages in the South American assemblage date to 16-17 my, those in the North American assemblage to 6-7 my. Few hummingbird-pollinated clades in either system have >4 species.
The asymmetric diversity build-up between hummingbirds and the plants dependent on them appears to arise not from rapid speciation within hummingbird-pollinated clades, but instead from a gradual and continuing process in which independent plant species switch from insect to bird pollination. Diversification within hummingbird-pollinated clades in the temperate regions of the Americas appears mainly due to habitat specialization and allopatric speciation, not bird pollination per se. Interaction tanglegrams, even if incomplete, indicate a lack of tight coevolution as perhaps expected for temperate-region mutualisms involving nectar-feeding vertebrates.
[Show abstract][Hide abstract] ABSTRACT: Dactylorhiza sambucina (L.) Soó is a polycarpic perennial herb. It is an element of the Central European, Eastern European, and Balkan floristic provinces of continental Europe. At the latter scale, D. sambucina is treated as a species of “least concern” by the IUCN. This paper deals with its taxonomic status, morphology, distribution, habitat requirements, mycorrhizal associations, and life cycle with special emphasis on reproduction. We also provide information on chromosome numbers and genetic variation. Our data from 12 years of monitoring D. sambucina in the Czech Republic show that three to four leaves have to be produced prior to flowering; plants with five and more leaves flower regularly. Juvenile plants near mother plants suggest recruitment from seeds. About 20% of 450 monitored plants underwent dormancy (failure of mature plants to produce above-ground parts in one or more growing seasons), the maximum duration being eight years. After reappearance, these individuals were mostly sterile for the next year. Mortality was highest (24%) at the seedling stage. Regarding the purple/yellow flower colour polymorphism so characteristic of D. sambucina, we found no correlation between morph frequency and soil properties (pH, calcium content), population density, or altitude above sea level.
Perspectives in Plant Ecology Evolution and Systematics 05/2015; in press(4). DOI:10.1016/j.ppees.2015.04.002 · 3.61 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Polyploidization can activate specific transposable elements, leading to their accumulation. At the same time, the preferential loss of repetitive elements in polyploids may be central to diploidization. The paucity of studies of transposable element (TE) dynamics in closely related diploid and polyploid species, however, prevents generalizations about these patterns. Here, we use low-coverage Illumina sequencing data for a clade of three tetraploid Orobanche species and a diploid relative to quantify the abundance and relative frequencies of different types of TEs. We confirmed tetraploidy in the sequenced individuals using standard cytogenetic methods and inferred the time of origin of the tetraploid clade with a rate-calibrated molecular clock.
The sequenced individuals of Orobanche austrohispanica, Orobanche densiflora, and Orobanche gracilis have 2n = 76 chromosomes, are tetraploid, and shared a most recent common ancestor some 6.7 Ma ago. Comparison of TE classifications from the Illumina data with classification from 454 data for one of the species revealed strong effects of sequencing technology on the detection of certain types of repetitive DNA. The three tetraploids show repeat enrichment especially of Gypsy TE families compared to eight previously analyzed Orobanchaceae. However, the diploid Orobanche rapum-genistae genome also has a very high proportion (30%) of Gypsy elements.
We had earlier suggested that tetraploidization might have contributed to an amplification of Gypsy elements, particularly of the Tekay clade, and that O. gracilis underwent genome downsizing following polyploidization. The new data reveal that Gypsy amplification in Orobanchaceae does not consistently relate to tetraploidy and that more species sampling is required to generalize about Tekay accumulation patterns.
Mobile DNA 03/2015; 6(5). DOI:10.1186/s13100-015-0034-8 · 2.11 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Background: Polyploidization can activate specific transposable elements, leading to their accumulation. At the same time, the preferential loss of repetitive elements in polyploids may be central to diploidization. The paucity of studies of transposable element (TE) dynamics in closely related diploid and polyploid species, however, prevents generalizations about these patterns. Here, we use low-coverage Illumina sequencing data for a clade of three tetraploid Orobanche species and a diploid relative to quantify the abundance and relative frequencies of different types of TEs. We confirmed tetraploidy in the sequenced individuals using standard cytogenetic methods and inferred the time of origin of the tetraploid clade with a rate-calibrated molecular clock. Findings: The sequenced individuals of Orobanche austrohispanica, Orobanche densiflora, and Orobanche gracilis have 2n = 76 chromosomes, are tetraploid, and shared a most recent common ancestor some 6.7 Ma ago. Comparison of TE classifications from the Illumina data with classification from 454 data for one of the species revealed strong effects of sequencing technology on the detection of certain types of repetitive DNA. The three tetraploids show repeat enrichment especially of Gypsy TE families compared to eight previously analyzed Orobanchaceae. However, the diploid Orobanche rapum-genistae genome also has a very high proportion (30%) of Gypsy elements. Conclusions: We had earlier suggested that tetraploidization might have contributed to an amplification of Gypsy elements, particularly of the Tekay clade, and that O. gracilis underwent genome downsizing following polyploidization. The new data reveal that Gypsy amplification in Orobanchaceae does not consistently relate to tetraploidy and that more species sampling is required to generalize about Tekay accumulation patterns.
[Show abstract][Hide abstract] ABSTRACT: Hornworts comprise ca. 220 species and are among the oldest landplant lineages, even though their precise phylogenetic position remains unclear. Deep within-hornwort divergences, highly uneven species numbers per genus, and the assumed high stem age together suggest a history of changing
diversification (i.e., speciation minus extinction) rates. To study the geographic distribution of modern hornworts and their patterns of species accumulation, we generated a mitochondrial and plastid DNA matrix for 103 species representing all major groups and then applied molecular-clock
dating, using a different calibration approach than in earlier work. We used the BAMM software to fit rate-variable and constant-rate birth-death diversification models to the dataset, and we also inferred ancestral areas to a time depth of 55 Ma (Early Eocene). We analyzed diversification
rates for all hornworts and separately for species-rich subclades. Under BAMM's variable-rates model (which fits the data better than a constant-rate birth-death model, but still assumes that each species has the same speciation and extinction probability regardless of its age), hornworts
have gradually increasing rates of speciation and a constant background extinction rate. No shifts in diversification rate could be detected. The implausible finding of a constant background extinction rate illustrates the limitations of diversification modeling especially as regards extinction
[Show abstract][Hide abstract] ABSTRACT: The monocot family Aponogetonaceae (Alismatales) consists only of Aponogeton, with 57 species occurring in Africa, Madagascar, India and Sri Lanka, Southeast Asia and Australia. Earlier studies inferred a Madagascan or Australian origin for the genus. Aponogeton-like pollen is documented from the Late Cretaceous of Wyoming, the early mid-Eocene of Canada, and the late mid-Eocene of Greenland. We obtained nuclear and plastid DNA sequences for 42 species and generated a time-calibrated phylogeny, rooted on appropriate outgroups. Statistical biogeographic analyses were carried out with or without the fossils incorporated in the phylogeny. The recent-most common ancestor of living Aponogetonaceae appears to date to the mid-Eocene and to have lived in Madagascar or Africa (but not Australia). Three transoceanic dispersal events from Africa/Madagascar to Asia sometime during the Miocene could explain the observed species relationships. As inferred in earlier studies, an ancient Australian species is sister to all other Aponogetonaceae, while the remaining Australian species stem from an Asian ancestor that arrived about 5 million years ago. The family’s ancient Northern Hemisphere fossil record and deepest extant divergence between a single Australian species and an Africa/Madagascar clade are statistically well-supported and rank among the most unusual patters in the biogeography of flowering plants.
[Show abstract][Hide abstract] ABSTRACT: Ant–plant symbioses involve over 110 ant species in five subfamilies that are facultative or obligate occupants of stem, leaf or root domatia formed by hundreds of ant-plant species. The phylogenetic distribution and geological ages of these associations, and the frequency of gains or losses of domatium, are largely unknown. We compiled an up-to-date list of ant domatium-bearing plants, estimated their probable true number from model-based statistical inference, generated dated phylogenies that include c. 50% of ant-plant lineages, and traced the occurrence of domatia and extrafloral nectaries on a 1181-species tree, using likelihood and Bayesian methods. We found 681 vascular plants with domatia (159 genera in 50 families) resulting from mini-mally 158 inferred domatium origins and 43 secondary losses over the last 19 Myr. The oldest African ant–plant symbioses are younger than those in Australasia and the Neotropics. The best statistical model suggests that the true number of myrmecophytes may approach 1140 species. The phylogenetic distribution of ant-plants shows that domatia evolved from a range of pre-adapted morphological structures and have been lost frequently, suggesting that domatia have no generalizable effect on diversification. The Miocene origin of ant–plant symbioses is consistent with inferred changes in diet and behaviour during ant evolution.
New Phytologist 01/2015; 207(2). DOI:10.1111/nph.13271 · 7.67 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: The family Caricaceae has six genera with together 34 species and one hybrid (Carvalho 2013). Besides the economically important crop, Carica papaya, other species in the family also produce edible fruits that are sold in local markets. The sister group of C. Papaya, which originated in Central America, consists of a clade of four species, three herbs in the genus Jarilla endemic to Mexico and Guatemala, and the single species of Horovitzia, H. cnidoscoloides, endemic to cloud forests of Sierra de Juarez in Oaxaca, southern Mexico (Carvalho and Renner 2012).
Molecular Phylogeny, Biogeography and an e-Monograph of the Papaya Family (Caricaceae) as an Example of Taxonomy in the Electronic Age, 01/2015: pages 83-92; , ISBN: 978-3-658-10266-1
[Show abstract][Hide abstract] ABSTRACT: A major concern in molecular clock dating is how to use information from the fossil record to calibrate genetic distances from DNA sequences. Here we apply three Bayesian dating methods that differ in how calibration is achieved-"node dating" (ND) in BEAST, "total evidence" (TE) dating in MrBayes, and the "fossilized birth-death" (FBD) in FDPPDiv-to infer divergence times in the royal ferns. Osmundaceae have 16-17 species in four genera, two mainly in the Northern Hemisphere and two in South Africa and Australasia; they are the sister clade to the remaining leptosporangiate ferns. Their fossil record consists of at least 150 species in ∼17 genera. For ND, we used the five oldest fossils, whereas for TE and FBD dating, which do not require forcing fossils to nodes and thus can use more fossils, we included up to 36 rhizomes and frond compression/impression fossils, which for TE dating were scored for 33 morphological characters. We also subsampled 10%, 25%, and 50% of the 36 fossils to assess model sensitivity. FBD-derived divergence ages were generally greater than those inferred from ND; two of seven TE-derived ages agreed with FBD-obtained ages, the others were much younger or much older than ND or FBD ages. We prefer the FBD-derived ages because they best fit the Osmundales fossil record (including Triassic fossils not used in our study). Under the preferred model, the clade encompassing extant Osmundaceae (and many fossils) dates to the latest Paleozoic to Early Triassic; divergences of the extant species occurred during the Neogene. Under the assumption of constant speciation and extinction rates, the FBD approach yielded speciation and extinction rates that overlapped those obtained from just neontological data. However, FBD estimates of speciation and extinction are sensitive to violations in the assumption of continuous fossil sampling; therefore, these estimates should be treated with caution.
[Show abstract][Hide abstract] ABSTRACT: In this Special feature, we assemble studies that illustrate phylogenetic approaches to studying salient questions regarding the effect of specialization on lineage diversification. The studies use an array of techniques involving a wide-ranging collection of biological systems (plants, butterflies, fish and amphibians are all represented). Their results reveal that macroevolutionary examination of specialization provides insight into the patterns of trade-offs in specialized systems; in particular, the genetic mechanisms of trade-offs appear to extend to very different aspects of life history in different groups. In turn, because a species may be a specialist from one perspective and a generalist in others, these trade-offs influence whether we perceive specialization to have effects on the evolutionary success of a lineage when we examine specialization only along a single axis. Finally, how geographical range influences speciation and extinction of specialist lineages remains a question offering much potential for further insight.
Proceedings of the Royal Society B: Biological Sciences 11/2014; 281(1795). DOI:10.1098/rspb.2014.2004 · 5.05 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: A striking example of plant/pollinator trait matching is found between Andean species of Passiflora with 6-14-cm-long nectar tubes and the sword-billed hummingbird, Ensifera ensifera, with up to 11-cm-long bills. Because of the position of their anthers and stigmas, and self-incompatibility, these passionflower species depend on E. ensifera for pollination. Field observations show that the bird and plant distribution match completely and that scarcity of Ensifera results in reduced passionflower seed set. We here use nuclear and plastid DNA sequences to investigate how often and when these mutualisms evolved and under which conditions, if ever, they were lost. The phylogeny includes 26 (70%) of the 37 extremely long-tubed species, 13 (68%) of the 19 species with tubes too short for Ensifera and four of the seven bat-pollinated species for a total of 43 (69%) of all species in Passiflora supersection Tacsonia (plus 11 outgroups). We time-calibrated the phylogeny to infer the speed of any pollinator switching. Results show that Tacsonia is monophyletic and that its stem group dates to 10.7 Ma, matching the divergence at 11.6 Ma of E. ensifera from its short-billed sister species. Whether pollination by short-billed hummingbirds or by Ensifera is the ancestral condition cannot be securely inferred, but extremely long-tubed flowers exclusively pollinated by Ensifera evolved early during the radiation of the Tacsonia clade. There is also evidence of several losses of Ensifera dependence, involving shifts to bat pollination and shorter billed birds. Besides being extremely asymmetric-a single bird species coevolving with a speciose plant clade-the Ensifera/Passiflora system is a prime example of a specialized pollinator not driving plant speciation, but instead being the precondition for the maintenance of isolated populations (through reliable seed set) that then underwent allopatric speciation.
Proceedings of the Royal Society B: Biological Sciences 11/2014; 281(1795). DOI:10.1098/rspb.2014.0888 · 5.05 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Premise of the study: Separating sexual function between different individuals carries risks, especially for sedentary organisms. Nevertheless, many land plants have unisexual gametophytes or sporophytes. This study brings together data and theoretical insights from research over the past 20 yr on the occurrence and frequency of plant sexual systems, focusing on the flowering plants. Methods: A list of genera with dioecious species, along with other information, is made available (http://www.umsl.edu/similar to renners/). Frequencies of other sexual systems are tabulated, and data on the genetic regulation, ecological context, and theoretical benefits of dioecy reviewed. Key results: There are 15 600 dioecious angiosperms in 987 genera and 175 families, or 5-6% of the total species (7% of genera, 43% of families), with somewhere between 871 to 5000 independent origins of dioecy. Some 43% of all dioecious angiosperms are in just 34 entirely dioecious clades, arguing against a consistent negative influence of dioecy on diversification. About 31.6% of the dioecious species are wind-pollinated, compared with 5.5-6.4% of nondioecious angiosperms. Also, 1.4% of all angiosperm genera contain dioecious and monoecious species, while 0.4% contain dioecious and gynodioecious species. All remaining angiosperm sexual systems are rare. Chromosomal sex determination is known from 40 species; environmentally modulated sex allocation is common. Few phylogenetic studies have focused on the evolution of dioecy. Conclusions: The current focus is on the genetic mechanisms underlying unisexual flowers and individuals. Mixed strategies of sexual and vegetative dispersal, together with plants' sedentary life style, may often favor polygamous systems in which sexually inconstant individuals can persist. Nevertheless, there are huge entirely dioecious clades of tropical woody plants.
American Journal of Botany 10/2014; 101(10):1588-96. DOI:10.3732/ajb.1400196 · 2.60 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Type specimens are permanently preserved biological specimens that fix the usage of species names. This method became widespread from 1935 onwards and is now obligatory.We used DNA sequencing of types and more recent collections of wild and cultivated melons to reconstruct the evolutionary history of the genus Citrullus and the correct names for its species.We discovered that the type specimen of the name Citrullus lanatus, prepared by a Linnaean collector in South Africa in 1773, is not the species now thought of as watermelon. Instead, it is a representative of another species that is sister to C. ecirrhosus, a tendril-less South African endemic. The closest relative of the watermelon instead is a West African species. Our nuclear and plastid data furthermore reveal that there are seven species of Citrullus, not four as assumed.Our study implies that sweet watermelon originates from West, not southern Africa as previously believed, and that the South African citron melon has been independently domesticated. These findings affect and explain numerous studies on the origin of these two crops that led to contradictory results because of the erroneous merging of several distinct species.
New Phytologist 10/2014; 205(2). DOI:10.1111/nph.13163 · 7.67 Impact Factor