Timing and tempo of early and successive adaptive radiations in Macaronesia

The flora of Macaronesia, which encompasses five Atlantic archipelagos (Azores, Canaries, Madeira, Cape Verde, and Salvage), is exceptionally rich and diverse. Spectacular radiation of numerous endemic plant groups has made the Macaronesian islands an outstanding area for studies of evolution and speciation. Despite intensive investigation in the last 15 years, absolute age and rate of diversification are poorly known for the flora of Macaronesia. Here we report molecular divergence estimates and rates of diversification for five representative, putative rapid radiations of monophyletic endemic plant lineages across the core eudicot clade of flowering plants. Three discrete windows of colonization during the Miocene and early Pliocene are suggested for these lineages, all of which are inferred to have had a single colonization event followed by rapid radiation. Subsequent inter-archipelago dispersal events into Madeira and the Cape Verdes took place very recently during the late Pliocene and Pleistocene after initial diversification on the Canary Islands. The tempo of adaptive radiations differs among the groups, but is relatively rapid compared to continental and other island radiations. Our results demonstrate that opportunity for island colonization and successful radiation may have been constrained to discrete time periods of profound climatic and geological changes in northern African and the Mediterranean.     

Frequent and parallel habitat transitions as driver of unbounded radiations in the Cape flora

The enormous species richness in the Cape Floristic Region (CFR) of Southern Africa is the result of numerous radiations, but the temporal progression and possible mechanisms of these radiations are still poorly understood. Here, we explore the macroevolutionary dynamics of the Restionaceae, which include 340 species that are found in all vegetation types in the Cape flora and are ecologically dominant in fynbos. Using an almost complete (i.e., 98%) species‐level time calibrated phylogeny and models of diversification dynamics, we show that species diversification is constant through the Cenozoic, with no evidence of an acceleration with the onset of the modern winter‐wet climate, or a recent density‐dependent slowdown. Contrary to expectation, species inhabiting the oldest (montane) and most extensive (drylands) habitats did not undergo higher diversification rates than species in the younger (lowlands) and more restricted (wetland) habitats. We show that the rate of habitat transitions is more closely related to the speciation rate than to time, and that more than a quarter of all speciation events are associated with habitat transitions. This suggests that the unbounded Restionaceae diversification resulted from numerous, parallel, habitat shifts, rather than persistence in a habitat stimulating speciation. We speculate that this could be one of the mechanisms resulting in the hyperdiverse Cape flora.     

Explaining the uniqueness of the Cape flora: incorporating geomorphic evolution as a factor for explaining its diversification

The plant diversity of the Cape Floristic Region is regarded as being exceptional in an ecological and evolutionary context. The region supports about double the number of species predicted by models based on water-energy variables for regional floras globally. However, contemporary diversity patterns are profoundly influenced by evolutionary processes contingent upon idiosyncrasies of history and geography. The relatively recent appearance of dated molecular phylogenies, and their optimization in relation to habitat and geography, has provided hitherto unsurpassed opportunities to generate knowledge about the evolution of the Cape flora. Almost all studies invoke climatic deterioration during the Mio-Pliocene as the major trigger of radiations and subsequent speciation of Cape clades. While some do show the importance of edaphic heterogeneity for clade radiation, the evolution of this heterogeneity is not considered. Here, we review the literature on the late Cenozoic geomorphic evolution of the Cape in order to assess the extent to which the changing nature of scenery and soils could act as a stimulus for plant diversification. Despite dating uncertainties associated with both the phylogenetic and geomorphic data, it appears that moderate uplift in the early and late Miocene, which significantly increased the topo-edaphic heterogeneity of the Cape was an important driver of plant diversification. In particular, the massive increase in heterogeneity after the late Miocene event probably acted in synergy with rapid climatic deterioration, to produce the extraordinarily rapid diversification recorded for some Cape clades at that time. A comparison of the plant diversity and palaeoenvironmetal patterns of mediterranean-climate regions provide insights regarding the "remarkable environmental conditions" of the Cape that have generated the high diversification and low extinction rates necessary to produce such a rich flora. These conditions are a gradual increase in topo-edaphic heterogeneity and relative climatic stability during the late Cenozoic.     

Do Mediterranean‐type ecosystems have a common history?—Insights from the Buckthorn family (Rhamnaceae)

Mediterranean‐type ecosystems (MTEs) are remarkable in their species richness and endemism, but the processes that have led to this diversity remain enigmatic. Here, we hypothesize that continent‐dependent speciation and extinction rates have led to disparity in diversity between the five MTEs of the world: the Cape, California, Mediterranean Basin, Chile, and Western Australia. To test this hypothesis, we built a phylogenetic tree for 280 Rhamnaceae species, estimated divergence times using eight fossil calibrations, and used Bayesian methods and simulations to test for differences in diversification rates. Rhamnaceae lineages in MTEs generally show higher diversification rates than elsewhere, but speciation and extinction dynamics show a pattern of continent‐dependence. We detected high speciation and extinction rates in California and significantly lower extinction rates in the Cape and Western Australia. The independent colonization of four of five MTEs may have occurred conterminously in the Oligocene/Early Miocene, but colonization of the Mediterranean Basin happened later, in the Late Miocene. This suggests that the in situ radiations of these clades were initiated before the onset of winter rainfall in these regions. These results indicate independent evolutionary histories of Rhamnaceae in MTEs, possibly related to the intensity of climate oscillations and the geological history of the regions.     

Ancient lakes as evolutionary reservoirs: evidence from the thalassoid gastropods of Lake Tanganyika

Ancient lakes are often collectively viewed as evolutionary hot spots of diversification. East Africa's Lake Tanganyika has long been the subject of scientific interest owing to dramatic levels of endemism in species as diverse as cichlid fishes, paludomid gastropods, decapod and ostracod crustaceans and poriferans. It is the largest and deepest of the African rift lakes, and its endemic fauna has been presented with a stable inland environment for over 10 Myr, offering unique opportunities for within-lake diversification. Although astonishing diversification has been documented in the endemic cichlid fauna of the lake, similar patterns of rapid diversification have long been assumed for other groups. In contrast to this hypothesis of rapid speciation, we show here that there has been no acceleration in the rate of speciation in the thalassoid gastropods of the lake following lake colonization. While limited within-lake speciation has occurred, the dramatic conchological diversity of gastropods presently found within the lake has evolved from at least four major lineages that pre-date its formation by as much as 40 Myr. At the same time, a widespread group of African gastropods appears to have evolved from taxa presently found in the lake. While Lake Tanganyika has been a cradle of speciation for cichlid fishes, it has also been an important evolutionary reservoir of gastropod lineages that have been extirpated outside the basin.     

Was it an explosion? Using population genetics to explore the dynamics of a recent radiation within Protea (Proteaceae L.)

Adaptive radiations likely underlie much of the world’s diversity, especially that of hyper‐diverse regions. They are usually characterized by a burst of speciation early in their evolutionary history, a pattern which can be detected using population genetic tools. The Cape Floristic Region (CFR) of southwestern South Africa is home to many spectacular plant radiations. Here, we investigate the white proteas (Protea section Exsertae), a typical CFR radiation, to determine if it demonstrates the burst of speciation associated with adaptive radiations in recent models. Inferences from individual assignment, tree‐based population relationships, and pairwise F‐statistics based on 10 microsatellite loci reveal that while the white proteas radiated recently they did not radiate explosively. In addition, we found evidence that there is little gene flow between sampled populations of most species. Taken together, these results demonstrate that within a small clade, the processes underlying the radiation are different from those envisioned by current models of adaptive radiation and suggest that geographical isolation could have played a role in the diversification of the group. Our study implicates both adaptive and non‐adaptive processes in the evolution of botanical diversity of the CFR.     

Plant species radiations: where,when, why?

The spatial and temporal patterns of plant species radiations are largely unknown. I used a nonlinear regression to estimate speciation and extinction rates from all relevant dated clades. Both are surprisingly high. A high species richness can be the result of either little extinction, thus preserving the diversity that dates from older radiations (a 'mature radiation'), or a 'recent and rapid radiation'. The analysis of radiations from different regions (Andes, New Zealand, Australia, southwest Africa, tropics and Eurasia) revealed that the diversity of Australia may be largely the result of mature radiations. This is in sharp contrast to New Zealand, where the flora appears to be largely the result of recent and rapid radiations. Mature radiations are characteristic of regions that have been climatically and geologically stable throughout the Neogene, whereas recent and rapid radiations are more typical of younger (Pliocene) environments. The hyperdiverse Cape and Neotropical floras are the result of the combinations of mature as well as recent and rapid radiations. Both the areas contain stable environments (the Amazon basin and the Cape Fold Mountains) as well as dynamic landscapes (the Andes and the South African west coast). The evolution of diversity can only be understood in the context of the local environment.     

Speciation and radiations track climate transitions since the Miocene Climatic Optimum: a case study of southern African chameleons

Aim The high amount of species diversity concentrated in southern Africa has been attributed to palaeoclimatic factors, and the timing of radiations in some taxa corresponds to global palaeoclimatic trends. Using dwarf chameleons (Bradypodion: Chamaeleonidae) as a model system, we explored the relationship between palaeoclimatic fluctuations and cladogenesis with respect to both temporal and spatial patterns in an effort to understand the process of speciation in southern Africa. Location South Africa, with particular emphasis on the Cape Floristic Region and the Maputaland–Pondoland–Albany hotspot. Methods Mitochondrial sequence data (ND2 and 16S) were used to estimate the timing of major radiations and to examine the number of lineages through time. A dated phylogeny was constructed using Bayesian phylogenetic reconstruction, and a Bayesian relaxed molecular clock was used to estimate divergence times. Spatial data and lineage‐through‐time plots were used to identify geographic regions that underwent diversification in connection with major climatic events. Both parsimony and likelihood optimizations of habitat type on the phylogeny were used to determine whether major habitat shifts have occurred. On a coarse scale (half‐degree grid cells), phylogenetic diversity (sum of the branch lengths linking terminals) was compared with species richness (absolute number of species) to identify areas of conservation importance. Results The complete species phylogeny of dwarf chameleons shows that the timing and mode of diversification exhibit spatio‐temporal patterns that link to phases in the evolution of southern Africa’s climate over the last 14 Myr. Optimizations of habitat on the phylogenetic tree show a progression from closed to open habitats since the Mid‐Miocene, corresponding to the shift from C₃ to C₄ environments, and later with the development of south‐western Africa’s winter‐rainfall regime. These shifts are not simultaneous across the region, with different geographic centres of diversity generated during different time periods. Main conclusions Regions that are prominent centres of chameleon diversification are encompassed by the current biodiversity hotspots as shown by chameleon species richness and phylogenetic diversity. Diversity within the Cape Floristic Region appears to be the result of a Late Pliocene radiation, whereas the diversity encompassed within the Maputaland–Pondoland–Albany hotspot is an aggregate of asynchronous radiation events, probably influenced by lineage losses. Overall, dwarf chameleons have experienced a shift in habitat types, with recent radiations occupying open habitats, and older lineages persisting in relictual forested habitats, corresponding to the continental shift of vegetation types since the Miocene Climatic Optimum.     

Primary controls on species richness in higher taxa

The disparity in species richness across the tree of life is one of the most striking and pervasive features of biological diversity. Some groups are exceptionally diverse, whereas many other groups are species poor. Differences in diversity among groups are frequently assumed to result from primary control by differential rates of net diversification. However, a major alternative explanation is that ecological and other factors exert primary control on clade diversity, such that apparent variation in net diversification rates is a secondary consequence of ecological limits on clade growth. Here, I consider a likelihood framework for distinguishing between these competing hypotheses. I incorporate hierarchical modeling to explicitly relax assumptions about the constancy of diversification rates across clades, and I propose several statistics for a posteriori evaluation of model adequacy. I apply the framework to a recent dated phylogeny of ants. My results reject the hypothesis that net diversification rates exert primary control on species richness in this group and demonstrate that clade diversity is better explained by total time-integrated speciation. These results further suggest that it may not possible to estimate meaningful speciation and extinction rates from higher-level phylogenies of extant taxa only.     

Continental faunal exchange and the asymmetrical radiation of carnivores

Lineages arriving on islands may undergo explosive evolutionary radiations owing to the wealth of ecological opportunities. Although studies on insular taxa have improved our understanding of macroevolutionary phenomena, we know little about the macroevolutionary dynamics of continental exchanges. Here we study the evolution of eight Carnivora families that have migrated across the Northern Hemisphere to investigate if continental invasions also result in explosive diversification dynamics. We used a Bayesian approach to estimate speciation and extinction rates from a substantial dataset of fossil occurrences while accounting for the incompleteness of the fossil record. Our analyses revealed a strongly asymmetrical pattern in which North American lineages invading Eurasia underwent explosive radiations, whereas lineages invading North America maintained uniform diversification dynamics. These invasions into Eurasia were characterized by high rates of speciation and extinction. The radiation of the arriving lineages in Eurasia coincide with the decline of established lineages or phases of climate change, suggesting differences in the ecological settings between the continents may be responsible for the disparity in diversification dynamics. These results reveal long-term outcomes of biological invasions and show that the importance of explosive radiations in shaping diversity extends beyond insular systems and have significant impact at continental scales.     

Phylogenetic analyses of Gammaridae crustacean reveal different diversification patterns among sister lineages in the Tethyan region

The Gammaridae shows the greatest disparity in species diversity and distribution pattern in the Amphipoda, with some genera ranging from the Palearctic to Nearctic, while others are limited to the Mediterranean region or ancient Tethyan margins. Here we present the first molecular phylogenetic analysis of the Gammaridae to investigate its evolutionary history using four genetic markers and a comprehensive set of taxa representing 198 species. The phylogenetic results revealed that the Gammaridae originated from the Tethyan region in the Cretaceous, and split into three morphologically and geographically distinct lineages by the end of the Paleocene. Diversification analysis combined with paleogeological evidence suggested that the Tethyan changes induced by sea‐level fluctuation and tectonic uplift triggered different diversification modes and range expansions for the three lineages. The Gammarus lineage underwent an early rapid radiation across Eurasia and North America, then declined towards modern species. Pontogammarids maintained stable diversification with restricted distributions around the Tethyan basin, whereas sarothrogammarids experienced evolutionary stasis by stranding on the ancient Tethyan margins. Our findings suggest that environmental changes have played an important role in the diversification of Gammaridae lineages, which could be an opportunity to promote adaptive radiations in new habitats, or constraints resulting in evolutionary relicts.     

Diversity versus disparity and the radiation of modern cetaceans

Modern whales are frequently described as an adaptive radiation spurred by either the evolution of various key innovations (such as baleen or echolocation) or ecological opportunity following the demise of archaic whales. Recent analyses of diversification rate shifts on molecular phylogenies raise doubts about this interpretation since they find no evidence of increased speciation rates during the early evolution of modern taxa. However, one of the central predictions of ecological adaptive radiation is rapid phenotypic diversification, and the tempo of phenotypic evolution has yet to be quantified in cetaceans. Using a time-calibrated molecular phylogeny of extant cetaceans and a morphological dataset on size, we find evidence that cetacean lineages partitioned size niches early in the evolutionary history of neocetes and that changes in cetacean size are consistent with shifts in dietary strategy. We conclude that the signature of adaptive radiations may be retained within morphological traits even after equilibrium diversity has been reached and high extinction or fluctuations in net diversification have erased any signature of an early burst of diversification in the structure of the phylogeny.     

A preliminary classification of evolutionary radiations

Rapid increases in taxonomic diversity are generally described as adaptive or evolutionary radiations. Such radiations differ widely in the rate and extent of morphologic innovation, taxonomic diversification and phylogenetic breadth, suggesting that several patterns, and likely processes, are involved. At least four distinct patterns of evolutionary radiation can be identified: novelty events, which generate new morphological complexity (altering the body plan of the group under consideration) but not necessarily with the associated production of many lower taxa; broad diversification events involving many independent lineages that undergo diversification, generate many new species and are driven by new ecological opportunities; economic radiations of a limited group of ecologically (but not necessarily phylogenetically) related clades exploiting a limited new ecologic opportunity; and adaptive radiations that may occur at any taxonomic level, but involve a rapid increase in diversity within a single clade, including “true”; adaptive radiations. Many events produce simple diversity increases with no corresponding increase in genetic/developmental/morphological/behavioral sophistication, but the most evolutionarily interesting events add new levels of complexity.     

Molecular evidence for ten species and Oligo-Miocene vicariance within a nominal Australian gecko species (<Emphasis Type="Italic">Crenadactylus ocellatus</Emphasis>, Diplodactylidae)

Background  

Molecular studies have revealed that many putative 'species' are actually complexes of multiple morphologically conservative, but genetically divergent 'cryptic species'. In extreme cases processes such as non-adaptive diversification (speciation without divergent selection) could mask the existence of ancient lineages as divergent as ecologically and morphologically diverse radiations recognised as genera or even families in related groups. The identification of such ancient, but cryptic, lineages has important ramifications for conservation, biogeography and evolutionary biology. Herein, we use an integrated multilocus genetic dataset (allozymes, mtDNA and nuclear DNA) to test whether disjunct populations of the widespread nominal Australian gecko species Crenadactylus ocellatus include distinct evolutionary lineages (species), and to examine the timing of diversification among these populations.     

Causes of plant diversification in the Cape biodiversity hotspot of South Africa

The Cape region of South Africa is one of the most remarkable hotspots of biodiversity with a flora comprising more than 9000 plant species, almost 70% of which are endemic, within an area of only ± 90,000 km2. Much of the diversity is due to an exceptionally large contribution of just a few clades that radiated substantially within this region, but little is known about the causes of these radiations. Here, we present a comprehensive analysis of plant diversification, using near complete species-level phylogenies of four major Cape clades (more than 470 species): the genus Protea, a tribe of legumes (Podalyrieae) and two speciose genera within the iris family (Babiana and Moraea), representing three of the seven largest plant families in this biodiversity hotspot. Combining these molecular phylogenetic data with ecological and biogeographical information, we tested key hypotheses that have been proposed to explain the radiation of the Cape flora. Our results show that the radiations started throughout the Oligocene and Miocene and that net diversification rates have remained constant through time at globally moderate rates. Furthermore, using sister-species comparisons to assess the impact of different factors on speciation, we identified soil type shifts as the most important cause of speciation in Babiana, Moraea, and Protea, whereas shifts in fire-survival strategy is the most important factor for Podalyrieae. Contrary to previous findings in other groups, such as orchids, pollination syndromes show a high degree of phylogenetic conservatism, including groups with a large number of specialized pollination syndromes like Moraea. We conclude that the combination of complex environmental conditions together with relative climatic stability promoted high speciation and/or low extinction rates as the most likely scenario leading to present-day patterns of hyperdiversity in the Cape.     

Exceptional among-lineage variation in diversification rates during the radiation of Australia's most diverse vertebrate clade

The disparity in species richness among groups of organisms is one of the most pervasive features of life on earth. A number of studies have addressed this pattern across higher taxa (e.g. 'beetles'), but we know much less about the generality and causal basis of the variation in diversity within evolutionary radiations at lower taxonomic scales. Here, we address the causes of variation in species richness among major lineages of Australia's most diverse vertebrate radiation, a clade of at least 232 species of scincid lizards. We use new mitochondrial and nuclear intron DNA sequences to test the extent of diversification rate variation in this group. We present an improved likelihood-based method for estimating per-lineage diversification rates from combined phylogenetic and taxonomic (species richness) data, and use the method in a hypothesis-testing framework to localize diversification rate shifts on phylogenetic trees. We soundly reject homogeneity of diversification rates among members of this radiation, and find evidence for a dramatic rate increase in the common ancestor of the genera Ctenotus and Lerista. Our results suggest that the evolution of traits associated with climate tolerance may have had a role in shaping patterns of diversity in this group.     

Diversification rate shifts in the Cape Floristic Region: The right traits in the right place at the right time

Species diversity patterns are the product of diversification rate variation, but the factors influencing changes in diversification rates are poorly known. Radiation is thought to be the result of ecological opportunity: the right traits in the right environment at the right time. We test this in the Cape Floristic Region (CFR) of South Africa, in which pyrophytic heathland (fynbos) and non-pyrophytic Afromontane forest occur interdigitated. We infer transitions from forest to fynbos in three Cape clades (Penaeaceae, Phyliceae and Diosmeae) and test if they are associated with diversification rate shifts and the evolution of functional traits linked to fire, high insolation and seasonal drought. We estimate diversification rate shifts using maximum likelihood and use phylogenetic comparative methods to show that forest to fynbos shifts were associated with decreases in leaf area and specific leaf area and preceded or coincided with increases in diversification rates. Furthermore, we show that Penaeaceae, Phyliceae and Diosmeae species are typical members of their vegetation types in terms of their traits. The diversification rate shifts of Penaeaceae and Phyliceae are dated to the Miocene, when postulated aridification-driven changes in the CFR fire regimes may have triggered expansion of the fynbos at the cost of forest, providing an ecological opportunity for the diversification of fynbos lineages.     

Parasitoid fig‐wasp evolutionary diversification and variation in ecological opportunity

Ecological processes are manifest in the evolution and form of phenotype diversity. The great abundance of parasitoid species has led to speculation whether rates of speciation and extinction are dependent on parasitoid diversity. If these factors are mutually exclusive, species diversity should fluctuate instead of remaining relatively constant over time. It is not known whether radiations constrained by coevolutionary interactions conform to density‐dependent diversification processes. Here we test the prediction that parasitoid fig wasp diversification responds to changes in ecological opportunity and density‐independent processes. A phylogenetic approach is used to estimate relative divergence times and infer diversification rate changes using γ‐statistics. Monte Carlo constant rates tests that accommodate incomplete sampling could not reject constant rates diversification. Parasitoid fig wasp diversification is consistent with a more complex explanation than density‐dependent cladogenesis. The results suggest contemporary African parasitoid fig wasp diversity remains a legacy of an ancient ecological opportunity facilitated by fig tree diversification following the breakup of Pan‐African forests and evolution of the savanna biome over the last 55 Ma and the more recent aridification of the African continent in the last 5 Ma. These results imply that amplified phenotypic differentiation of specialist insects coevolving with plants is coupled to evolutionarily infrequent changes in ecological opportunity.     

Loss of sexual recombination and segregation is associated with increased diversification in evening primroses

The loss of sexual recombination and segregation in asexual organisms has been portrayed as an irreversible process that commits asexually reproducing lineages to reduced diversification. We test this hypothesis by estimating rates of speciation, extinction, and transition between sexuality and functional asexuality in the evening primroses. Specifically, we estimate these rates using the recently developed BiSSE (Binary State Speciation and Extinction) phylogenetic comparative method, which employs maximum likelihood and Bayesian techniques. We infer that net diversification rates (speciation minus extinction) in functionally asexual evening primrose lineages are roughly eight times faster than diversification rates in sexual lineages, largely due to higher speciation rates in asexual lineages. We further reject the hypothesis that a loss of recombination and segregation is irreversible because the transition rate from functional asexuality to sexuality is significantly greater than zero and in fact exceeded the reverse rate. These results provide the first empirical evidence in support of the alternative theoretical prediction that asexual populations should instead diversify more rapidly than sexual populations because they are free from the homogenizing effects of sexual recombination and segregation. Although asexual reproduction may often constrain adaptive evolution, our results show that the loss of recombination and segregation need not be an evolutionary dead end in terms of diversification of lineages.     

Rapid cladogenesis in marine fishes revisited

Lineages that underwent rapid cladogenesis are attractive systems for the study of mechanisms underlying taxonomic, ecological, morphological, and behavioral diversification. Recently developed statistical methods provide insights into historical patterns of diversity and allow distinguishing bursts of cladogenesis from stochastic background rates in the presence of confounding factors such as extinction and incomplete taxon sampling. Here, we compare the dynamics of speciation in several marine fish lineages some of which were previously proposed to have undergone significant changes of cladogenesis through time. We tested for evidence of episodes of rapid cladogenesis using the constant rate and Monte Carlo constant rate tests that are robust to incomplete taxon sampling. These tests employ the statistic gamma to measure the relative position of internal node in a chronogram. For the first time, we conducted a comparative analysis to address the behavior of the statistic under different chronogram-constructing methods (Langley-Fitch, nonparametric rate smoothing, and penalized likelihood). Although estimates of gamma sometimes differ widely among methods, acceptance or rejection of the constant rate model within a particular clade appears to be robust to the choice of method. Bursts of cladogenesis were detected in 14 of 34 studied datasets. Some of these were previously proposed to represent marine fish "radiations," whereas others are identified anew. Our results indicate that the wider application of tree shape methods that are able to detect significantly elevated rates of speciation is useful to more precisely define clades that underwent episodes of rapid cladogenesis in marine fish clades. Contrasting the patterns of phylogenetic diversification in marine fish lineages may facilitate the identification of common evolutionary trajectories versus idiosyncrasies, and ultimately help towards a better understanding of the factors and processes underlying speciation in the marine realm.