Diversification rates in the Australasian endemic grass Austrostipa: 15 million years of constant evolution

Plastid phylogenomics provides new insights into the systematics, diversification, and biogeography of Cymbidium (Orchidaceae)

Aim The family Rutaceae (rue family) is the largest within the eudicot order Sapindales and is distributed mainly in the tropical and subtropical regions of both the New World and the Old World, with a few genera in temperate zones. The main objective of this study is to present molecular dating and biogeographical analyses of the subfamily Spathelioideae, the earliest branching clade (which includes eight extant genera), to interpret the temporal and spatial origins of this group, ascertaining possible vicariant patterns and dispersal routes and inferring diversification rates through time.Location Pantropics.Methods A dataset comprising a complete taxon sampling at generic level (83.3% at species level) of Spathelioideae was used for a Bayesian molecular dating analysis (beast). Four fossil calibration points and an age constraint for Sapindales were applied. An ancestral area reconstruction analysis utilizing the dispersal–extinction–cladogenesis model and diversification rate analyses was conducted.Results Dating analyses indicate that Rutaceae and Spathelioideae are probably of Late Cretaceous origin, after which Spathelioideae split into a Neotropical and a Palaeotropical lineage. The Palaeotropical taxa have their origin inferred in Africa, with postulated dispersal events to the Mediterranean, the Canary Islands, Madagascar and Southeast Asia. The lineages within Spathelioideae evolved at a relatively constant diversification rate. However, abrupt changes in diversification rates are inferred from the beginning of the Miocene and during the Pliocene/Pleistocene.Main conclusions The geographical origin of Spathelioideae probably lies in Africa. The existence of a Neotropical lineage may be the result of a dispersal event at a time in the Late Cretaceous when South America and Africa were still quite close to each other (assuming that our age estimates are close to the actual ages), or by Gondwanan vicariance (assuming that our age estimates provide minimal ages only). Separation of land masses caused by sea level changes during the Pliocene and Pleistocene may have been triggers for speciation in the Caribbean genus Spathelia.

AimThe Mediterranean Basin (MB) is a species‐rich biogeographical region with many endemic taxa. We analysed the historical patterns of temporal and geographical diversification of Mediterranean Blaps (Tenebrionidae), a diverse group of flightless beetles, estimated their date of origin and colonization of the MB, and tracked temporal changes in diversification rates.LocationMediterranean Basin.MethodsWe reconstructed the phylogenetic relationships of Mediterranean Blaps using four mitochondrial genes and 47 morphological characters. Divergence‐time estimates were investigated with a Bayesian relaxed clock approach that was calibrated with both fossil and geological constraints. Biogeographical analyses were performed using the dispersal–extinction–cladogenesis likelihood model associated with a stratified palaeogeographical scenario. Diversification rate analyses allowed the investigation of diversity dynamics through time as well as rate shifts during major Cenozoic climate events.ResultsThe Bayesian relaxed clock analysis suggests that Blaps first appeared in the MB about 28 Ma. The most likely scenario is that Mediterranean Blaps originated in the Arabian and north‐east African regions and then dispersed progressively westwards and northwards, using temporary land bridges to colonize the northern shores of the MB. Island endemics are more likely to be the products of recent dispersals than of old vicariance events. Birth–death analyses suggest that diversification rates in the Miocene and Pliocene are consistent with a ‘museum model’, in which most of the extant diversity is best explained by a steady accumulation of lineages under constant diversification rates. Although major Cenozoic climatic events do not seem to have influenced the diversification of Mediterranean Blaps, a decrease in diversification rates was detected during the Pleistocene.Main conclusionsOur results suggest that Mediterranean Blaps lineages diversified between the Oligocene and the Pliocene, with current distribution patterns mostly accounted for by early vicariance and late dispersal events. Diversification rates were relatively constant through time, but decreased during Pleistocene glaciation cycles. This scenario may be applicable to other Mediterranean terrestrial animal taxa.

AimShifts in diversification rates of Australian flora and fauna have been associated with aridification, but the relationship between diversification rates and aridity has never been quantified. We employed multiple approaches to reconstruct paleoenvironments of Australia for the first time. We used this information, and phylogenetic‐based analyses, to explore how changes in temperature and increasing aridity during the Neogene influenced the diversification of the Australian blindsnakes. We tested whether diversification rates differ between arid‐adapted and mesic‐adapted lineages.TaxonTyphlopidae, Anilios blindsnakes.LocationAustralia.Materials and MethodsWe estimated the historical biogeography of blindsnakes using BioGeoBEARS. We synthesised multiple approaches to reconstruct paleotemperature and paleoaridity of Australia during the Neogene. We fitted several birth‐death models and estimated diversification rates under paleoenvironmental conditions using RPANDA. We further compared diversification rates between arid‐adapted lineages versus mesic‐adapted lineages using ClaDS and GeoHiSSE.ResultsAncestral area estimation indicated Australian blindsnakes have tropical grassland origins. We found that Australia‐specific regional paleotemperature and paleoaridity provided a better explanation for diversification rate variation than global paleotemperature. Specifically, our best‐fitting model indicated that speciation rates of blindsnakes decreased with increasing aridity. We found no difference in diversification rates between arid‐ and mesic‐adapted lineages.Main ConclusionsSoon after dispersing to Australia, the common ancestors of Australian blindsnakes diversified rapidly in mesic habitats during the early Miocene. However, as the continent became increasingly arid, diversification rates decreased. We found that shifts in the environment led to the emergence of two major clades: one remaining in primarily mesic habitats and the other adapting to the expanding arid biome. Our results emphasise the importance of both arid and tropical biomes as sources and sinks of diversification.

Colonisation of new geographic regions and/or of new ecological resources can result in rapid species diversification into the new ecological niches available. Members of the subgenus Drosophila are distributed across the globe and show a large diversity of ecological niches. Furthermore, taxonomic classification of Drosophila includes the rank radiation, which refers to closely related species groups. Nevertheless, it has never been tested if these taxonomic radiations correspond to evolutionary radiations. Here we present a study of the patterns of diversification of Drosophila to test for increased diversification rates in relation to the geographic and ecological diversification processes. For this, we have estimated and dated a phylogeny of 218 species belonging to the major species groups of the subgenus. The obtained phylogenies are largely consistent with previous studies and indicate that the major groups appeared during the Oligocene/Miocene transition or early Miocene, characterized by a trend of climate warming with brief periods of glaciation. Ancestral reconstruction of geographic ranges and ecological resource use suggest at least two dispersals to the Neotropics from the ancestral Asiatic tropical disribution, and several transitions to specialized ecological resource use (mycophagous and cactophilic). Colonisation of new geographic regions and/or of new ecological resources can result in rapid species diversification into the new ecological niches available. However, diversification analyses show no significant support for adaptive radiations as a result of geographic dispersal or ecological resource shift. Also, cactophily has not resulted in an increase in the diversification rate of the repleta and related groups. It is thus concluded that the taxonomic radiations do not correspond to adaptive radiations.

BackgroundPhylogenetic hypotheses are increasingly being used to elucidate historical patterns of diversification rate-variation. Hypothesis testing is often conducted by comparing the observed vector of branching times to a null, pure-birth expectation. A popular method for inferring a decrease in speciation rate, which might suggest an early burst of diversification followed by a decrease in diversification rate is the γ statistic.MethodologyUsing simulations under varying conditions, I examine the sensitivity of γ to the distribution of the most recent branching times. Using an exploratory data analysis tool for lineages through time plots, tree deviation, I identified trees with a significant γ statistic that do not appear to have the characteristic early accumulation of lineages consistent with an early, rapid rate of cladogenesis. I further investigated the sensitivity of the γ statistic to recent diversification by examining the consequences of failing to simulate the full time interval following the most recent cladogenic event. The power of γ to detect rate decrease at varying times was assessed for simulated trees with an initial high rate of diversification followed by a relatively low rate.ConclusionsThe γ statistic is extraordinarily sensitive to recent diversification rates, and does not necessarily detect early bursts of diversification. This was true for trees of various sizes and completeness of taxon sampling. The γ statistic had greater power to detect recent diversification rate decreases compared to early bursts of diversification. Caution should be exercised when interpreting the γ statistic as an indication of early, rapid diversification.

AimThe accumulation of supraspecific lineages in Asia has been linked to climatic changes and tectonic events starting in the Miocene, but few studies have extended the intraspecific history of relict plants in subtropical China back to the Early or Middle Miocene. In this study, we investigate the effects of events from the late Early Miocene onwards on the evolutionary history of a relict plant, Cyclocarya paliurus, in subtropical China.LocationSubtropical China.MethodsSequence variation in two chloroplast intergenic spacers (atpB–rbcL and psbA–trnH) and one nuclear gene (PHYA) was investigated across 57 populations of C. paliurus. Standard population genetic analyses, estimation of the most recent common ancestor of chloroplast haplotypes and diversification rate analyses were carried out, and Bayesian skyline plots were constructed.ResultsThe time to the most recent common ancestor of all 17 chloroplast haplotypes in C. paliurus was 16.69 Ma (95% HPD 8.42–27.86 Ma), which largely coincides with the initial intensification of the Asian monsoon and global climate cooling during the Early to Middle Miocene. Chloroplast lineage diversification started to increase in the early Late Miocene, with peaks at c. 9.6 Ma and c. 3.6 Ma, corresponding temporally to two subsequent intensification events of the Asian monsoon. Bayesian skyline plots of both markers revealed that C. paliurus could have experienced at least two waves of expansion since the middle Pleistocene. The distributions of chlorotypes and clades were both consistent with a multiple‐refugia model but with strong signals of range expansion.Main conclusionsThis study provides a long evolutionary profile of an archaic plant species in subtropical China, dating from the late Early Miocene. Our results suggest that the occurrence of the Asian monsoon and associated tectonic events, as well as Pleistocene climate changes, had a pervasive influence on the phylogeographical structure of plants in subtropical China.

Mesozoic origin of coleoid cephalopods and their abrupt shifts of diversification patterns

Abstract. Ancient lakes represent key ecosystems for endemic freshwater species. This high endemic biodiversity has been shown to be mainly the result of intra-lacustrine diversification. Whereas the principle role of this mode of diversification is generally acknowledged, actual diversification rates in ancient lakes remain little understood. At least four types are conceivable. Diversification rates may be constant over time, they may fluctuate, rates may be higher in the initial phase of diversification, or there may be a pronounced lag phase between colonization and subsequent diversification. As understanding the tempo of diversification in ancient lake environments may help reveal the underlying processes that drive speciation and extinction, we here use the Balkan Lake Ohrid as a model system and the largest species flock in the lake, the non-pyrgulinid Hydrobiidae, as a model taxon to study changes in diversification rates over time together with the respective drivers. Based on phylogenetic, molecular-clock, lineage-through-time plot, and diversification-rate analyses we found that this potentially monophyletic group is comparatively old and that it most likely evolved with a constant diversification rate. Preliminary data of the SCOPSCO (Scientific Collaboration On Past Speciation Conditions in Lake Ohrid) deep-drilling program do indicate signatures of severe environmental/climatic perturbations in Lake Ohrid. However, so far there is no evidence for the occurrence of catastrophic environmental events. We therefore propose that the constant diversification rate observed in endemic gastropods has been caused by two factors: (i) a potential lack of catastrophic environmental events in Lake Ohrid and/or (ii) a probably high ecosystem resilience, buffering environmental changes. Parameters potentially contributing to the lake's high ecosystem resilience are its distinct bathymetry, ongoing tectonic activities, and karst hydrology. The current study not only contributes to one of the overall goals of the SCOPSCO deep-drilling program – inferring the driving forces for biotic evolution in Lake Ohrid. It might also enhance our understanding of how ecosystem resilience, in general, may promote relatively constant diversification rates in isolated ecosystems. However, we encourage future studies testing hypotheses about the lack of catastrophic events in Lake Ohrid. These studies should be based on high-resolution data for the entire geological history of the lake, and they should potentially involve information from the sediment fossil record, not only for gastropods but also for other groups with a high share of endemic taxa.

Aim To investigate the effects of Pleistocene climatic variations on the diversification rate of the subgenus Calathus (Coleoptera: Carabidae), and to estimate the role of vicariance and dispersal for explaining current distributional patterns.Location Western Palaearctic Region, particularly the Mediterranean Basin.Methods Fragments of the mitochondrial cox1–cox2 and the nuclear 28S and EF1α genes were analysed by Bayesian inference. Lineage divergence times were estimated using a Bayesian relaxed molecular clock. Three diversification rate analyses were conducted, namely gamma (γ)‐statistic, birth–death likelihood (BDL) test and survival analyses, in order to test departures from a constant rate model of diversification. A Bayesian approach to dispersal–vicariance analysis was developed to reconstruct the most probable ancestral area of subgenus Calathus and subsequent events of dispersal and colonization.Results A constant rate of speciation events from the late Miocene onwards was found for the subgenus Calathus, whereas recent Pleistocene climatic oscillations played an important role only in shaping intraspecific diversity. Overall diversification patterns for the subgenus are best explained by at least four westward dispersal events from the eastern Mediterranean Basin. Three distinct phylogroups were found for the widely distributed Calathus fuscipes. Incongruence between mitochondrial and nuclear loci was found for a number of species.Main conclusions Diversification analyses suggest either a constant rate of diversification (BDL analysis) or a decrease in diversification rates for the subgenus (survival or γ‐statistics analyses), but not an increase related to the effects of glaciation cycles. Diversification patterns in the subgenus Calathus agree with predictions of the taxon pulse model. From the middle Miocene onwards the Anatolian Peninsula was possibly the main centre of diversification, with successive dispersal events towards the western Mediterranean Basin. Range expansion and secondary contact zones are postulated between members of different phylogroups in C. fuscipes.

AimTo reconstruct the spatio‐temporal evolution of Fosterella (Bromeliaceae), a genus characterized by a high degree of endemism in the Central Andes, and to account for contemporary patterns of diversity and distribution within the genus.LocationFosterella has its centre of diversity in the Central Andes (24 species), where it occurs in two major biomes: the Yungas and seasonally dry tropical forests (SDTF). The genus displays three major disjunctions: Amazonia (one species), Central America (one species), and the Brazilian Shield (five species).MethodsPhylogenetic relationships within Fosterella were inferred based on six plastid DNA regions. Parsimony and likelihood methods, a Bayesian relaxed molecular clock, ancestral area reconstructions, and diversification rate analyses were used to infer the spatio‐temporal evolution of Fosterella.ResultsThe origin of extant lineages of Fosterella was placed in the late Miocene (c. 9.6 Ma) during the last rapid Andean uplift. SDTF and azonal lowland sites were inferred as the most likely ancestral habitats. The Yungas were colonized several times independently from c. 4.7 Ma onwards. Only one clade diversified in the Yungas, indicative of an ecological shift to moister and cooler conditions. Two recent long‐distance dispersals to Central America and to Amazonia were inferred. Diversification rates within Fosterella were found to be constant through time and comparatively low (0.4 species Myr−1).Main conclusionsAllopatric speciation is the main mode of diversification in Fosterella. The isolated distribution of suitable habitats fostered the evolution of a high degree of endemism. The low speciation rates in Fosterella contrast with high diversification rates of Andean high‐elevation taxa but are similar to other Andean low‐ to mid‐elevation taxa. The last rapid Andean uplift did not leave a detectable signature in the diversification rates of Fosterella.

Reappraising adaptive radiation

Molecular phylogenies and historical biogeography of a circumtropical group of gastropods (Genus: Nerita): Implications for regional diversity patterns in the marine tropics

Between the late Oligocene and the early Miocene, climatic changes have shattered the faunal and floral communities and drove the apparition of new ecological niches. Grassland biomes began to supplant forestlands, thus favouring a large-scale ecosystem turnover. The independent adaptive radiations of several mammal lineages through the evolution of key innovations are classic examples of these changes. However, little is known concerning the evolutionary history of other herbivorous groups in relation with this modified environment. It is especially the case in phytophagous insect communities, which have been rarely studied in this context despite their ecological importance. Here, we investigate the phylogenetic and evolutionary patterns of grass-specialist moths from the species-rich tribe Apameini (Lepidoptera, Noctuidae). The molecular dating analyses carried out over the corresponding phylogenetic framework reveal an origin around 29 million years ago for the Apameini. Ancestral state reconstructions indicate (i) a potential Palaearctic origin of the tribe Apameini associated with a major dispersal event in Afrotropics for the subtribe Sesamiina; (ii) a recent colonization from Palaearctic of the New World and Oriental regions by several independent lineages; and (iii) an ancestral association of the tribe Apameini over grasses (Poaceae). Diversification analyses indicate that diversification rates have not remained constant during the evolution of the group, as underlined by a significant shift in diversification rates during the early Miocene. Interestingly, this age estimate is congruent with the development of grasslands at this time. Rather than clade ages, variations in diversification rates among genera better explain the current differences in species diversity. Our results underpin a potential adaptive radiation of these phytophagous moths with the family Poaceae in relation with the major environmental shifts that have occurred in the Miocene.

Maximum likelihood is a potentially powerful approach for investigating the tempo of diversification using molecular phylogenetic data. Likelihood methods distinguish between rate-constant and rate-variable models of diversification by fitting birth-death models to phylogenetic data. Because model selection in this context is a test of the null hypothesis that diversification rates have been constant over time, strategies for selecting best-fit models must minimize Type I error rates while retaining power to detect rate variation when it is present. Here I examine model selection, parameter estimation, and power to reject the null hypothesis using likelihood models based on the birth-death process. The Akaike information criterion (AIC) has often been used to select among diversification models; however, I find that selecting models based on the lowest AIC score leads to a dramatic inflation of the Type I error rate. When appropriately corrected to reduce Type I error rates, the birth-death likelihood approach performs as well or better than the widely used gamma statistic, at least when diversification rates have shifted abruptly over time. Analyses of datasets simulated under a range of rate-variable diversification scenarios indicate that the birth-death likelihood method has much greater power to detect variation in diversification rates when extinction is present. Furthermore, this method appears to be the only approach available that can distinguish between a temporal increase in diversification rates and a rate-constant model with nonzero extinction. I illustrate use of the method by analyzing a published phylogeny for Australian agamid lizards.