H. Peter Linder

Phylogenetic biome conservatism on a global scale

How and why organisms are distributed as they are has long intrigued evolutionary biologists. The tendency for species to retain their ancestral ecology has been demonstrated in distributions on local and regional scales, but the extent of ecological conservatism over tens of millions of years and across continents has not been assessed. Here we show that biome stasis at speciation has outweighed biome shifts by a ratio of more than 25:1, by inferring ancestral biomes for an ecologically diverse sample of more than 11,000 plant species from around the Southern Hemisphere. Stasis was also prevalent in transocean colonizations. Availability of a suitable biome could have substantially influenced which lineages establish on more than one landmass, in addition to the influence of the rarity of the dispersal events themselves. Conversely, the taxonomic composition of biomes has probably been strongly influenced by the rarity of species’ transitions between biomes. This study has implications for the future because if clades have inherently limited capacity to shift biomes, then their evolutionary potential could be strongly compromised by biome contraction as climate changes.

Rapid and recent origin of species richness in the Cape flora of South Africa

The Cape flora of South Africa grows in a continental area with many diverse and endemic species. We need to understand the evolutionary origins and ages of such ‘hotspots’ to conserve them effectively. In volcanic islands the timing of diversification can be precisely measured with potassium–argon dating. In contrast, the history of these continental species is based upon an incomplete fossil record and relatively imprecise isotopic palaeotemperature signatures. Here we use molecular phylogenetics and precise dating of two island species within the same clade as the continental taxa to show recent speciation in a species-rich genus characteristic of the Cape flora. The results indicate that diversification began approximately 7–8 Myr ago, coincident with extensive aridification caused by changes in ocean currents. The recent origin of endemic species diversity in the Cape flora shows that large continental bursts of speciation can occur rapidly over timescales comparable to those previously associated with oceanic island radiations.

Origin and diversification of the Greater Cape flora: Ancient species repository, hot-bed of recent radiation, or both?

Like island-endemic taxa, whose origins are expected to postdate the appearance of the islands on which they occur, biome-endemic taxa should be younger than the biomes to which they are endemic. Accordingly, the ages of biome-endemic lineages may offer insights into biome history. In this study, we used the ages of multiple lineages to explore the origin and diversification of two southern African biomes whose remarkable floristic richness and endemism has identified them as global biodiversity hotspots (succulent karoo and fynbos). We used parsimony optimization to identify succulent karoo- and fynbos-endemic lineages across 17 groups of plants, for which dated phylogenies had been inferred using a relaxed Bayesian (BEAST) approach. All succulent karoo-endemic lineages were less than 17.5 My old, the majority being younger than 10 My. This is largely consistent with suggestions that this biome is the product of recent radiation, probably triggered by climatic deterioration since the late Miocene. In contrast, fynbos-endemic lineages showed a broader age distribution, with some lineages originating in the Oligocene, but most being more recent. Also, in groups having both succulent karoo- and fynbos-endemic lineages, there was a tendency for the latter to be older. These patterns reflect the greater antiquity of fynbos, but also indicate considerable recent speciation, probably through a combination of climatically-induced refugium fragmentation and adaptive radiation.

A fundamental, eco‐hydrological basis for niche segregation in plant communities

• Ecologists still puzzle over how plant species manage to coexist with one another while competing for the same essential resources. The classic answer for animal communities is that species occupy different niches, but how plants do this is more difficult to determine. We previously found niche segregation along fine-scale hydrological gradients in European wet meadows and proposed that the mechanism might be a general one, especially in communities that experience seasonal saturation. • We quantified the hydrological niches of 96 species from eight fynbos communities in the biodiversity hotspot of the Cape Floristic Region, South Africa and 99 species from 18 lowland wet meadow communities in the UK. Niche overlap was computed for all combinations of species. • Despite the extreme functional and phylogenetic differences between the fynbos and wet meadow communities, an identical trade-off (i.e. specialization of species towards tolerance of aeration and/or drying stress) was found to cause segregation along fine-scale hydrological gradients. • This study not only confirms the predicted generality of hydrological niche segregation, but also emphasizes its importance for structuring plant communities. Eco-hydrological niche segregation will have implications for conservation in habitats that face changing hydrology caused by water abstraction and climate change.

The Cape element in the Afrotemperate flora: from Cape to Cairo?

The build-up of biodiversity is the result of immigration and in situ speciation. We investigate these two processes for four lineages (Disa, Irideae p.p., the Pentaschistis clade and Restionaceae) that are widespread in the Afrotemperate flora. These four lineages may be representative of the numerous clades which are species rich in the Cape and also occur in the highlands of tropical Africa. It is as yet unclear in which direction the lineages spread. Three hypotheses have been proposed: (i) a tropical origin with a southward migration towards the Cape, (ii) a Cape origin with a northward migration into tropical Africa, and (iii) vicariance. None of these hypotheses has been thoroughly tested. We reconstruct the historical biogeography of the four lineages using likelihood optimization onto molecular phylogenies. We find that tropical taxa are nested within a predominantly Cape clade. There is unidirectional migration from the Cape into the Drakensberg and from there northwards into tropical Africa. The amount of in situ diversification differs between areas and clades. Dating estimates show that the migration into tropical East Africa has occurred in the last 17 Myr, consistent with the Mio-Pliocene formation of the mountains in this area.

Polyphyly of Arundinoideae (Poaceae): Evidence from rbcL Sequence Data

Sequence data from the plastid encoded gene rbcL are used to determine phylogenetic relationships between various lineages in the grasses, with particular emphasis on the subfamily Arundinoideae. Thirty four sequences, producing 155 phylogenetically informative sites, were analysed using both parsimony and distance methods. Cladistic analyses indicate that there are two main lineages: Pooideae (including the Stipeae) and a large clade comprising Panicoideae, Arun- dinoideae, Chloridoideae, and Centothecoideae. The Bambusoideae are unresolved and basal to these two lineages. Relationships within the panicoid, arundinoid, chloridoid, and centothecoid clade indicate that Arundinoideae as presently circumscribed are paraphyletic, as lineages within this subfamily show affinities with all three of the other subfamilies. Despite poor support for some relationships, rbcL appears to be well suited for systematic studies in the Poaceae.

MACROEVOLUTIONARY DATA SUGGEST A ROLE FOR REINFORCEMENT IN POLLINATION SYSTEM SHIFTS

Abstract Reproductive isolation can evolve either as a by-product of divergent selection or through reinforcement. We used the Cape flora of South Africa, known for its high level of pollination specialization, as a model system to test the potential role of shifts in pollination system in the speciation process. Comparative analysis of 41 sister-species pairs (representing Geraniaceae, Iridaceae, and Orchidaceae) for which complete pollinator, edaphic, and distribution data are available showed that for sister species with overlapping distribution ranges, pollination system shifts are significantly associated with edaphic shifts. In contrast, there is no significant association between pollination system shifts and edaphic shifts for allopatric sister species. These results are interpreted as evidence for reinforcement.

CONTRASTING PATTERNS OF RADIATION IN AFRICAN AND AUSTRALIAN RESTIONACEAE

Abstract The floras of the Mediterranean‐climate areas of southern Africa and southwestern Australia are remarkably species rich. Because the two areas are at similar latitudes and in similar positions on their respective continents, they have probably had similar Cenozoic climatic histories. Here we test the prediction that the evolution of the species richness in the two areas followed a similar temporal progression by comparing the rates of lineage accumulation for African and Australian Restionaceae. Restionaceae (Poales) are typical and often dominant elements in the fynbos vegetation of the Cape Floristic Region of southern Africa and the kwongan vegetation of the Southwestern Floristic Province of Western Australia. The phylogeny of the family was estimated from combined datasets for rbcL and trnL‐F sequences and a large morphological dataset; these datasets are largely congruent. The monophyly of Restionaceae is supported and a basal division into an African clade (˜ 350 species) and an Australian clade (146 species) corroborated. There is also support for a futher subdivision of these two large sister‐clades, but the terminal resolution within the African clade is very weak. Fossil pollen records provided a minimum age of the common ancestor of Australian and African Restionaceae as 64–71 million years ago, and this date was used to calibrate a molecular clock. A molecular clock was rejected by a likelihood ratio test; therefore, rate changes between the lineages were smoothed using nonparametric rate smoothing. The rate‐corrected ages were used to construct a plot of lineages through time. During the Palaeogene the Australian lineage diversity increased consistent with the predictions of the constant birthrate model, while the African lineage diversity showed a dramatic increase in diversification rate in the Miocene. Incomplete sampling obscures the patterns in the Neogene, but extending the trends to the modern extant diversity suggests that this acceleration in the speciation rate continued in the African clade, whereas the Australian clade retained a constant diversification rate. The substantial morphological and anatomical similarity between the African and Australian Restionaceae appear to preclude morphological innovations as possible explanations for the intercontinental differences. Most likely these differences are due to the greater geographical extent and ecological variation in temperate Australia than temperate Africa, which might have provided refugia for basal Restionaceae lineages, whereas the more mountainous terrain of southern Africa might have provided the selective regimes for a more rapid, recent speciation.

Intraspecific Variability and Timing in Ancestral Ecology Reconstruction: A Test Case from the Cape Flora

Thamnochortus (ca. 32 species) is an ecologically diverse genus of Restionaceae. Restionaceae comprise a major component of the southern African Cape flora, wherein eco-diversification might have been important in the generation of high levels of species richness. In an attempt to reconstruct the macroecological history of Thamnochortus, it was found that standard procedures for character state optimization make two inappropriate assumptions. The first is that ancestors are monomorphic (i.e., ecologically uniform) and the second is that eco-diversification follows, or is slower than, lineage diversification. We demonstrate a variety of coding schemes with which the assumption of monomorphy can be avoided. For unordered discrete ecological characters, presence coding and generalized frequency coding (GFC) are suboptimal because they occasionally yield illogical assignments of no state to ancestors. Polymorphism coding or use of the program DIVA are preferable in this respect but are applicable only with parsimony. For continuous eco-characters (e.g., a rainfall gradient, where individual species occur in ranges), GFC and MaxMin coding provide equally valid solutions to optimizing ranges with parsimony. However, MaxMin can be extended to likelihood approaches and is therefore preferable. With respect to rates and timing, all algorithms currently employed for ancestral ecology reconstruction bias toward slow rates of eco-diversification relative to lineage diversification. An alternative to this bias is provided by DIVA, which biases toward accelerated rates of eco-diversification and thus inferences of ecology-driven speciation. We see no way of choosing between these biases; however, phylogeneticists should be aware of them. Applying these methods to Thamnochortus, we find there to be important differences in details, yet general congruence, regarding the historical ecology of this clade. We infer the most recent common ancestor of Thamnochortus to have been a post-fire resprouting species distributed on rocky, well-drained, sandstone-derived soils at lower-middle elevations, in regions of moderate levels of yearly (primarily winter) rainfall. This species would have been distributed in habitats much like those of the southwestern Cape mountains today. Major ecological trends include shifts to lower rainfall regimes and shifts from sandstone to limestone-derived alkaline soils at lower altitudes.

CONTRASTING FLOWERING PHENOLOGY AND SPECIES RICHNESS IN ABIOTICALLY AND BIOTICALLY POLLINATED ANGIOSPERMS

Abstract Biotic pollination is thought to correlate with increased interspecific competition for pollination among plants and a higher speciation rate. In this study we compared patterns of flowering phenology and species richness between abiotically (wind) and biotically pollinated plants, using phylogenetically independent contrasts. We compiled phenological data from eight local seasonal floras, in which we found geographically overlapping sister clades. Of 65 documented origins of wind pollination, we were able to use up to 17 independent contrasts. In contrast to previous studies we found no difference in global species richness between wind‐ and biotically pollinated sister clades. Regarding phenology, we found wider phenological spread in biotically pollinated clades, earlier flowering onset in wind‐pollinated trees, but no difference in duration of flowering between pollination modes. These results corroborate previous views that niche space is more constrained for wind‐pollinated species, and that niche partitioning is less important between wind‐pollinated plants compared to plants pollinated by animals.