Diversification Shifts Research Articles

Phylogenomics recovers multiple origins of portable case making in caddisflies (Insecta: Trichoptera), nature's underwater architects.

Caddisflies (Trichoptera) are among the most diverse groups of freshwater animals with more than 16 000 described species. They play a fundamental role in freshwater ecology and environmental engineering in streams, rivers and lakes. Because of this, they are frequently used as indicator organisms in biomonitoring programmes. Despite their importance, key questions concerning the evolutionary history of caddisflies, such as the timing and origin of larval case making, remain unanswered owing to the lack of a well-resolved phylogeny. Here, we estimated a phylogenetic tree using a combination of transcriptomes and targeted enrichment data for 207 species, representing 48 of 52 extant families and 174 genera. We calibrated and dated the tree with 33 carefully selected fossils. The first caddisflies originated approximately 295 million years ago in the Permian, and major suborders began to diversify in the Triassic. Furthermore, we show that portable case making evolved in three separate lineages, and shifts in diversification occurred in concert with key evolutionary innovations beyond case making.

Testing extinction events and temporal shifts in diversification and fossilization rates through the skyline Fossilized Birth-Death (FBD) model: The example of some mid-Permian synapsid extinctions.

In the last decade, the Fossilized Birth-Death (FBD) process has yielded interesting clues about the evolution of biodiversity through time. To facilitate such studies, we extend our method to compute the probability density of phylogenetic trees of extant and extinct taxa in which the only temporal information is provided by the fossil ages (i.e. without the divergence times) in order to deal with the piecewise constant FBD process, known as the "skyline FBD", which allows rates to change between pre-defined time intervals, as well as modelling extinction events at the bounds of these intervals. We develop approaches based on this method to assess hypotheses about the diversification process and to answer questions such as "Does a mass extinction occur at this time?" or "Is there a change in the fossilization rate between two given periods?". Our software can also yield Bayesian and maximum-likelihood estimates of the parameters of the skyline FBD model under various constraints. These approaches are applied to a simulated dataset in order to test their ability to answer the questions above. Finally, we study an updated dataset of Permo-Carboniferous synapsids to get additional insights into the dynamics of biodiversity change in three clades (Ophiacodontidae, Edaphosauridae and Sphenacodontidae) in the Pennsylvanian (Late Carboniferous) and Cisuralian (Early Permian), and to assess support for end-Sakmarian (or Artinskian) and end-Cisuralian mass extinction events discussed in previous studies.

Locomotion and the early Mesozoic success of Archosauromorpha.

The Triassic was a time of ecological upheaval as life recovered from the Permian-Triassic mass extinction. Archosauromorphs were a key component of the recovery, diversifying substantially during the Triassic and encompassing the origins of dinosaurs, pterosaurs and crocodylomorphs. Here, we explore the evolution of locomotion in Archosauromorpha to test whether dinosaurs show any distinctive locomotory features that might explain their success. We implement geometric morphometrics on limb bone shapes and use limb ratios to calculate bipedality and cursoriality metrics. We find that the Avemetatarsalia (dinosaurs, pterosaurs and relatives) exhibit more variable limb form and limb ratios than any other group, indicating a wider range of locomotory modes. The earliest avemetatarsalians were bipedal and cursorial, and their range of form increased through the Triassic with notable diversification shifts following extinction events. This is especially true of dinosaurs, even though these changes cannot be discriminated from a stochastic process. By contrast, the Pseudosuchia (crocodilians and relatives) were more restricted in limb form and locomotor mode with disparity decreasing through time, suggesting more limited locomotor adaptation and vulnerability to extinction. Perhaps the greater locomotor plasticity of dinosaurs gave them a competitive advantage in the changing climates of the Late Triassic.

Revisiting phylogeny, systematics, and biogeography of a Pleistocene radiation.

Pilosocereus (Cactaceae) is an important dry forest element in all subregions and transitional zones of the neotropics, with the highest diversity in eastern Brazil. The genus is subdivided into informal taxonomic groups; however, most of these are not supported by recent molecular phylogenetic inferences. This lack of confidence is probably due to the use of an insufficient number of loci and the complexity of cactus diversification. Here, we explored the species relationships in Pilosocereus in more detail, integrating multilocus phylogenetic approaches with the assessment of the ancestral range and the effect of geography on diversification shifts. We used 28 nuclear, plastid, and mitochondrial loci from 54 plant samples of 31 Pilosocereus species for phylogenetic analyses. We used concatenated and coalescent phylogenetic trees and Bayesian models to estimate the most likely ancestral range and diversification shifts. All Pilosocereus species were clustered in the same branch, except P. bohlei. The phylogenetic relationships were more associated with the geographic distribution than taxonomic affinities among taxa. The genus began diversifying during the Plio-Pleistocene transition in the Caatinga domain and experienced an increased diversification rate during the Calabrian age. We recovered a well-supported multispecies coalescent phylogeny. Our results refine the pattern of rapid diversification of Pilosocereus species across neotropical drylands during the Pleistocene and highlight the need for taxonomic rearrangements in the genus. We recovered a pulse of diversification during the Pleistocene that was likely driven by multiple dispersal and vicariance events within and among the Caatinga, Cerrado, and Atlantic Forest domains.

Evolutionary timescale of chalcidoid wasps inferred from over one hundred mitochondrial genomes.

Chalcidoidea is one of the most biologically diverse groups among Hymenoptera. Members are characterized by extraordinary parasitic lifestyles and extensive host ranges, among which several species attack plants or serve as pollinators. However, higher-level chalcidoid relationships remain controversial. Here, we performed mitochondrial phylogenomic analyses for major clades (18 out of 25 families) of Chalcidoidea based on 139 mitochondrial genomes. The compositional heterogeneity and conflicting backbone relationships in Chalcidoidea were assessed using various datasets and tree inferences. Our phylogenetic results supported the monophyly of 16 families and polyphyly of Aphelinidae and Pteromalidae. Our preferred topology recovered the relationship (Mymaridae+(Signiphoridae+Leucospidae)+(Chalcididae+((Perilampidae+Eucharitidae)+ remaining Chalcidoidea)))). The monophyly of Agaonidae and Sycophaginae was rejected, while the gall-associated ((Megastigmidae+Ormyridae)+(Ormocerinae+Eurytomidae)) relationship was supported in most results. A six-gene inversion may be a synapomorphy for most families, whereas other derived gene orders may introduce confusion in phylogenetic signals at deeper nodes. Dating estimates suggested that Chalcidoidea arose near the Jurassic/Cretaceous boundary and that two dynamic shifts in diversification occurred during the evolution of Chalcidoidea. We hypothesized that the potential codiversification between chalcidoids and their hosts may be crucial for accelerating the diversification of Chalcidoidea. Ancestral state reconstruction analyses supported the hypothesis that gall-inducers were mainly derived from parasitoids of gall-inducers, while other gall-inducers were derived from phytophagous groups. Taken together, these findings advance our understanding of mitochondrial genome evolution in the major interfamilial phylogeny of Chalcidoidea.

Ecologically diverse island-associated lizard radiation shows idiosyncratic trait diversification shifts and homogenous speciation dynamics

A key area of interest in evolutionary biology has been understanding the role of ecological opportunity in the formation of adaptive radiations, lineages where speciation and phenotypic diversification are driven by open ecological opportunity. Evolutionary theory posits that adaptive radiations should show initial bursts of ecomorphological diversification and rapid speciation, and that these two processes are correlated. Here, we investigate and contrast these predictions across ecomorphologically diverse continental (Australia) and insular (New Caledonia and New Zealand) radiations of diplodactyloid geckos. We test two key hypotheses: (a) that island colonization and the transition to novel niche-space has resulted in increased rates of speciation and trait diversification and (b) that rates of morphological diversification are correlated across multiple trait axes. Surprisingly, we find that speciation rate is homogenous and morphological diversification rates are idiosyncratic and uncorrelated with speciation rates. Tests of morphological integration suggests that while all traits coevolve, constraint may act differentially on individual axes. This accords with a growing number of studies indicating that ecologically diverse and species-rich radiations can show limited or no evidence of exceptional regime shifts in speciation dynamics or morphological diversification, especially in continental contexts.

The significance of recent diversification in the Northern Hemisphere in shaping the modern global flora revealed from the herbaceous tribe of Rubieae (Rubiaceae)

The global herbaceous flora is probably shaped by both ancient and/or recent diversification, companied with the impacts from geographic differences between the Northern and Southern Hemispheres. Therefore, its biogeographic pattern with respect to temporal and spatial divergence is far from full understanding. Tribe Rubieae, the largest herbaceous tribe in the woody-dominant Rubiaceae, provides an excellent opportunity for studying the macroevolution of worldwide colonization. Here, we aim to reconstruct the evolutionary history of Rubieae with regard to climate fluctuation and geological history in the Cenozoic. A total of 204 samples of Rubieae representing all the distribution areas of the tribe were used to infer its phylogenetic and biogeographic histories based on two nrDNA and six cpDNA regions. The ancestral area of Rubieae was reconstructed using a time-calibrated phylogeny in RASP and diversification rates were inferred using Bayesian analysis of macroevolutionary mixtures (BAMM). Our results show Rubieae probably originated in European region during the middle Oligocene, with the two subtribes separating at 26.8 million years ago (Ma). All the genera in Rubieae formed separate clades between 24.79 and 6.23 Ma. The ancestral area of the subtribe Rubiinae was the Madrean-Tethyan plant belt and the North Atlantic land bridge (NALB) provided passage between North America and Europe for Rubiinae. The subtribe Galiinae clade originated in Europe/central Asia during the late Oligocene. Two diversification shifts were detected within Rubieae in the late Neogene. Most extant Rubieae species diverged recently during the Neogene within clades that generally were established during the late Paleogene. The tribe shows complex migration/dispersal patterns within the North Hemisphere combined with multiple recent dispersals into Southern Hemisphere. Our results highlighted the important role of recent biogeographic diversification in the Northern Hemisphere in shaping the modern global herbaceous flora during the latest and rapid worldwide expansion in the Neogene.

So Volcanoes Created the Dinosaurs? A Quantitative Characterization of the Early Evolution of Terrestrial Pan-Aves

The early Mesozoic is marked by several global-scale environmental events, including the emplacement of large igneous provinces, such as the Siberian Traps, Wrangellia, and Central Atlantic Magmatic Province (CAMP). These have been hypothesised as drivers of the successful diversification of Pan-Aves, the lineage of archosaurs closer to birds than to crocodiles. We characterize here the diversification and body size evolution of terrestrial pan-avians (excluding pterosaurs) along the Triassic and Early Jurassic, using phylogenetic- and occurrence-based approaches, in an attempt to test the influence of such drivers. As diversity metrics, we quantified raw species richness and phylogenetic diversity (using time-calibrated phylogenetic trees), and net diversification rates were estimated with PyRate and the episodic fossilized-birth-death model. We have also characterised through-time patterns of body size (femoral length) and estimated body size evolutionary rates. Our results indicate that macroevolutionary shifts estimated from occurrence data are placed more recently in time than those from phylogenetic-based approaches, as shown by the higher diversity increase, diversification rates, and body size disparity of terrestrial Pan-Aves in the Carnian. This is consistent with hypotheses suggesting that the Carnian Pluvial Episode (CPE) was crucial for the early radiation of the group. Yet, phylogeny-based results show higher diversity/diversification rates for the Ladinian and Norian, suggesting a minor effect for the Carnian Pluvial Episode (CPE). We also found no meaningful shifts in diversity, diversification, or size-related metrics across the Triassic-Jurassic boundary. Even if the end-Triassic mass extinction possibly emptied ecospace, allowing dinosaur diversity to increase during the Jurassic, our results suggest that this expansion did not occur fast and homogeneously for the entire group. In fact, a sustained reduction in diversity and sub-zero net diversification rates are seen after the extinction, but macroevolutionary patterns here should be interpreted with care towards the end of the Early Jurassic, as they may be biased by an “edge effect.” Overall, few macroevolutionary shifts were consistently identified across all results, suggesting that the early diversification of terrestrial pan-avians was more nuanced and complex than anticipated.

Onset of Late Cretaceous diversification in Europe\u2019s freshwater gastropod fauna links to global climatic and biotic events

The Mesozoic rise of the European freshwater gastropod fauna is still poorly understood. Compared to the well documented Cenozoic history, little is known about the patterns and processes underlying the early diversification preceding their extinction crisis at the K–Pg boundary. We assess what is probably a first pulse of diversification of the Cenozoic-type fauna in the Late Cretaceous along with the potential abiotic and biotic controls for shifts in species diversification. We find strong support that the increase in the speciation rate in the Santonian (~ 85 Myr ago) is linked to a global sea level rise, which caused extensive flooding of continental areas and the formation of vast brackish-water ecosystems. The following decline of the speciation rate coincides with a rise in diversity and reflects increasing interspecific competition. The peak in the speciation rate postdates the Cenomanian–Turonian Thermal Maximum, which probably limited the potential for diversification among freshwater gastropods due to ecological constraints. The peak coincides moreover with the end phase of the Cretaceous Terrestrial Revolution, which sparked the radiation of angiosperms. The expansion and diversification of flowering plants, being an important food source for freshwater gastropods today, could have formed a necessary basis for gastropod diversification.

Probabilities of tree topologies with temporal constraints and diversification shifts

Dating the tree of life is a task far more complicated than only determining the evolutionary relationships between species. It is therefore of interest to develop approaches apt to deal with undated phylogenetic trees. The main result of this work is a method to compute probabilities of undated phylogenetic trees under Markovian diversification models by constraining some of the divergence times to belong to given time intervals and by allowing diversification shifts on certain clades. If the diversification models considered are lineage-homogeneous, the time complexity of this computation is quadratic with the number of species of the phylogenetic tree and linear with the number of temporal constraints. The interest of this computation method is illustrated with three applications, namely, to compute the distribution of the divergence times of a tree topology with temporal constraints, to directly sample the divergence times of a tree topology, and to test for a diversification shift at a given clade.

Molecular phylogeny and macroevolution of Chaitophorinae aphids (Insecta: Hemiptera: Aphididae)

AbstractChaitophorinae is a predominantly Northern Hemisphere aphid subfamily characterized by numerous setae on the body. Two constituent tribes are associated with different host plants, with Chaitophorini feeding on deciduous trees and shrubs and Siphini colonizing grasses. Based on data from multiple genes (COI, COII, Cytb and EF‐1α), geographical distribution and host association, this study investigated the phylogeny and macroevolution of Chaitophorinae using phylogenetic reconstruction, molecular dating, model‐based ancestral area and character estimations and diversification rate calculation. Our results support the monophyly of Chaitophorinae and two tribes, indicate that Sipha and the two largest genera Chaitophorus and Periphyllus are not monophyletic, and suggest a need for a change in the taxonomic status of Lambersaphis, which was nested within Chaitophorus in the phylogenetic tree. We recovered an origin of Chaitophorinae on Acer plants from eastern Asia during the Late Cretaceous to early Palaeocene, followed by multiple dispersals into other areas that were responsible for its contemporary distribution. The origins of Siphini and Chaitophorus + Lambersaphis coincided with colonizations of novel host plants. An increase in diversification rate occurred within Chaitophorus in the Miocene and was associated with range expansion and switching onto new host plants, highlighting the roles of dispersal and host shift in aphid diversification.

Influence of historical changes in tropical reef habitat on the diversification of coral reef fishes

Past environmental changes are expected to have profoundly impacted diversity dynamics through time. While some previous studies showed an association between past climate changes or tectonic events and important shifts in lineage diversification, it is only recently that past environmental changes have been explicitly integrated in diversification models to test their influence on diversification rates. Here, we used a global reconstruction of tropical reef habitat dynamics during the Cenozoic and phylogenetic diversification models to test the influence of (i) major geological events, (ii) reef habitat fragmentation and (iii) reef area on the diversification of 9 major clades of tropical reef fish (Acanthuridae, Balistoidea, Carangoidea, Chaetodontidae, Haemulinae, Holocentridae, Labridae, Pomacentridae and Sparidae). The diversification models revealed a weak association between paleo-habitat changes and diversification dynamics. Specifically, the fragmentation of tropical reef habitats over the Cenozoic was found to be a driver of tropical reef fish diversification for 2 clades. However, overall, our approach did not allow the identification of striking associations between diversification dynamics and paleo-habitat fragmentation in contrast with theoretical model’s predictions.

Gene duplications and phylogenomic conflict underlie major pulses of phenotypic evolution in gymnosperms.

Inferring the intrinsic and extrinsic drivers of species diversification and phenotypic disparity across the tree of life is a major challenge in evolutionary biology. In green plants, polyploidy (or whole-genome duplication, WGD) is known to play a major role in microevolution and speciation, but the extent to which WGD has shaped macroevolutionary patterns of diversification and phenotypic innovation across plant phylogeny remains an open question. Here, we examine the relationship of various facets of genomic evolution-including gene and genome duplication, genome size, and chromosome number-with macroevolutionary patterns of phenotypic innovation, species diversification, and climatic occupancy in gymnosperms. We show that genomic changes, such as WGD and genome-size shifts, underlie the origins of most major extant gymnosperm clades, and notably, our results support an ancestral WGD in the gymnosperm lineage. Spikes of gene duplication typically coincide with major spikes of phenotypic innovation, while increased rates of phenotypic evolution are typically found at nodes with high gene-tree conflict, representing historic population-level dynamics during speciation. Most shifts in gymnosperm diversification since the rise of angiosperms are decoupled from putative WGDs and instead are associated with increased rates of climatic occupancy evolution, particularly in cooler and/or more arid climatic conditions, suggesting that ecological opportunity, especially in the later Cenozoic, and environmental heterogeneity have driven a resurgence of gymnosperm diversification. Our study provides critical insight on the processes underlying diversification and phenotypic evolution in gymnosperms, with important broader implications for the major drivers of both micro- and macroevolution in plants.

Universal probabilistic programming offers a powerful approach to statistical phylogenetics

Statistical phylogenetic analysis currently relies on complex, dedicated software packages, making it difficult for evolutionary biologists to explore new models and inference strategies. Recent years have seen more generic solutions based on probabilistic graphical models, but this formalism can only partly express phylogenetic problems. Here, we show that universal probabilistic programming languages (PPLs) solve the expressivity problem, while still supporting automated generation of efficient inference algorithms. To prove the latter point, we develop automated generation of sequential Monte Carlo (SMC) algorithms for PPL descriptions of arbitrary biological diversification (birth-death) models. SMC is a new inference strategy for these problems, supporting both parameter inference and efficient estimation of Bayes factors that are used in model testing. We take advantage of this in automatically generating SMC algorithms for several recent diversification models that have been difficult or impossible to tackle previously. Finally, applying these algorithms to 40 bird phylogenies, we show that models with slowing diversification, constant turnover and many small shifts generally explain the data best. Our work opens up several related problem domains to PPL approaches, and shows that few hurdles remain before these techniques can be effectively applied to the full range of phylogenetic models.

Habitat preference and diversification rates in a speciose lineage of diving beetles

The long-term geological stability of aquatic habitats has been demonstrated to be a determinant in the evolution of macroinvertebrate fauna, with species in running (lotic) waters having lower dispersal abilities, smaller ranges and higher gene flow between populations than species in standing (lentic) environments. Lotic species have been hypothesized to be more specialised, but the diversification dynamics of both habitat types have not been studied in detail. Using a speciose lineage of water beetles we test here whether diversification rates are related to the habitat preference of the species and its consequences on turnover, which we expect to be higher for lotic taxa. Moreover, we tested whether life in lotic environments is acting as an evolutionary dead-end as it is considered an ecological specialisation. We built a comprehensive molecular phylogeny with 473 terminals representing 421 of the 689 known species of the tribe Hydroporini (Coleoptera, Dytiscidae), using a combination of sequences from four mitochondrial and two nuclear genes plus 69 mitogenomes obtained with NGS. We found a general pattern of gradual acceleration of diversification rate with time, with 2–3 significant diversification shifts. However, habitat is not the main factor driving diversification in Hydroporini based on SecSSE analyses. The most recent common ancestor of Hydroporini was reconstructed as a lotic species, with multiple shifts to lentic environments. Most frequent transitions were estimated from lentic and lotic habitats to the category “both”, followed by transitions from lotic to lentic and lentic to lotic respectively, although with very similar rates. Contrary to expectations, we found little evidence for differences in diversification dynamics between habitats, with lotic environments clearly not acting as evolutionary dead-ends in Hydroporini.

Phylogeny, divergence times, and diversification in Calophyllaceae: Linking key characters and habitat changes to the evolution of Neotropical Calophylleae

The clusioid clade comprises five monophyletic families: Bonnetiaceae, Calophyllaceae, Clusiaceae s.s., Hypericaceae, and Podostemaceae. Even though the circumscription of these families is well established, phylogenetic relationships within some families remain unresolved. This study aims to infer phylogenetic relationships within the Neotropical Calophylleae based on a broad sampling of taxa and a multilocus approach. We then use our phylogenetic framework as basis to investigate the evolution and biogeography of Calophylleae and diversification shifts in Calophyllaceae. To reconstruct the phylogeny of the Neotropical Calophylleae, we used five plastid (matK, ndhF, rbcL, psbA-trnH, and trnK), two mitochondrial (matR and rps3), and two nuclear (EMB2765 and ITS) markers, including previously published and newly generated sequences. We sampled 74 species, increasing sampling of Neotropical taxa by 500%. Our phylogenetic hypothesis for Calophyllaceae provides additional support for the monophyly of all genera and allowed us to identify four main clades: Calophyllum, Kayea, Mammea, and the Neotropical clade. The Neotropical clade includes three main lineages, a small clade composed of Clusiella and Marila, and a large HaCaKi clade (i.e., Haplocarpa, Caraipa, and Kilmeyera) that is sister to Mahurea exstipulata. The evolution of three morphological traits (i.e., fleshy fruits, anther glands, and winged seeds) were shown to be associated with changes in evolutionary dynamics in Calophyllaceae, while a biome shift was detected in Kielmeyera, affecting net diversification within this genus. Major geological and climatic events such as the Andean uplift and a gradual decrease in temperatures seem to have influenced diversification rates within the Neotropical Calophylleae.

Molecules and Fossils Tell Distinct Yet Complementary Stories of Mammal Diversification

Reconstructing how biodiversity arose is a fundamental goal of evolutionary biologists. Yet whether the fossil record or time-calibrated phylogenies of living species yield comparable evolutionary rate estimates is controversial, and possibly affected by the temporal scale of question being asked. Here we investigate diversification timing across mammals by comparing rate signatures in a credible set of molecular timetrees (N =5,911 species, ~ 70% from DNA) to those in fossil genus durations (N =5,262). Fossil-corrected and timetree-based rate estimates begin converging ~23 million years ago (Ma) and are equal at the present, in accord with progressively fewer unsampled extinctions ‘pulling’ on the timetree rates toward the present to cause underestimates. ‘Pushing’ the pulled timetree rates by means of fossil-recorded extinctions identifies a major pulse of speciation ~60 Ma, soon after the Cretaceous-Paleogene mass extinction event, due to the radiation of fossil stem lineages. For groups without substantial fossil records, all is not lost, however. We show that species-specific ‘tip’ rates of speciation are unbiased estimators of recent evolutionary processes; in turn, the clade-level skewness of tip rates approximates the extent of past shifts in net diversification. Molecular timetrees need fossil-correction to address deep-time questions, but timetrees are sufficient for shallower time questions for which extinctions are fewer and ecological diversity can be fully sampled.

The roles of wing color pattern and geography in the evolution of Neotropical Preponini butterflies.

Diversification rates and evolutionary trajectories are known to be influenced by phenotypic traits and the geographic history of the landscapes that organisms inhabit. One of the most conspicuous traits in butterflies is their wing color pattern, which has been shown to be important in speciation. The evolution of many taxa in the Neotropics has also been influenced by major geological events. Using a dated, species‐level molecular phylogenetic hypothesis for Preponini, a colorful Neotropical butterfly tribe, we evaluated whether diversification rates were constant or varied through time, and how they were influenced by color pattern evolution and biogeographical events. We found that Preponini originated approximately 28 million years ago and that diversification has increased through time consistent with major periods of Andean uplift. Even though some clades show evolutionarily rapid transitions in coloration, contrary to our expectations, these shifts were not correlated with shifts in diversification. Involvement in mimicry with other butterfly groups might explain the rapid changes in dorsal color patterns in this tribe, but such changes have not increased species diversification in this group. However, we found evidence for an influence of major Miocene and Pliocene geological events on the tribe's evolution. Preponini apparently originated within South America, and range evolution has since been dynamic, congruent with Andean geologic activity, closure of the Panama Isthmus, and Miocene climate variability.

Detecting Lineage-Specific Shifts in Diversification: A Proper Likelihood Approach.

The branching patterns of molecular phylogenies are generally assumed to contain information on rates of the underlying speciation and extinction processes. Simple birth–death models with constant, time-varying, or diversity-dependent rates have been invoked to explain these patterns. They have one assumption in common: all lineages have the same set of diversification rates at a given point in time. It seems likely, however, that there is variability in diversification rates across subclades in a phylogenetic tree. This has inspired the construction of models that allow multiple rate regimes across the phylogeny, with instantaneous shifts between these regimes. Several methods exist for calculating the likelihood of a phylogeny under a specified mapping of diversification regimes and for performing inference on the most likely diversification history that gave rise to a particular phylogenetic tree. Here, we show that the likelihood computation of these methods is not correct. We provide a new framework to compute the likelihood correctly and show, with simulations of a single shift, that the correct likelihood indeed leads to parameter estimates that are on average in much better agreement with the generating parameters than the incorrect likelihood. Moreover, we show that our corrected likelihood can be extended to multiple rate shifts in time-dependent and diversity-dependent models. We argue that identifying shifts in diversification rates is a nontrivial model selection exercise where one has to choose whether shifts in now-extinct lineages are taken into account or not. Hence, our framework also resolves the recent debate on such unobserved shifts. [Diversification; macroevolution; phylogeny; speciation]

How important is it to consider lineage diversification heterogeneity in macroevolutionary studies? Lessons from the lizard family Liolaemidae

AbstractMacroevolutionary and biogeographical studies commonly apply multiple models to test state‐dependent diversification. These models track the association between states of interest along a phylogeny, although many of them do not consider whether different clades might be evolving under different evolutionary drivers. Yet, they are still commonly applied to empirical studies without careful consideration of possible lineage diversification heterogeneity along the phylogenetic tree. A recent biogeographic study has suggested that orogenic uplift of the southern Andes has acted as a species pump, driving diversification of the lizard family Liolaemidae (307 described species), native to temperate southern South America. Here, we argue against the Andean uplift as main driver of evolution in this group. We show that there is a clear pattern of heterogeneous diversification in the Liolaemidae, which biases state‐ and environment‐dependent analyses in, respectively, the GeoSSE and RPANDA programs. We show here that there are two shifts to accelerated speciation rates involving two clades that have both been classified as having “Andean” distributions. We incorporated the Geographic Hidden‐State Speciation and Extinction model (GeoHiSSE) to accommodate unrelated diversification shifts, and also re‐analyzed the data in RPANDA program after splitting biologically distinct clades for separate analyses, as well as including a more appropriate set of models. We demonstrate that the “Andean uplift” hypothesis is not supported when the heterogeneous diversification histories among these lizards is considered. We use the Liolaemidae as an ideal system to demonstrate potential risks of ignoring clade‐specific differences in diversification patterns in macroevolutionary studies. We also implemented simulations to show that, in agreement with previous findings, the HiSSE approach can effectively and substantially reduce the level of distribution‐dependent models receiving the highest AIC weights in such scenarios. However, we still find a relatively high rate (15%) of distribution‐dependent models receiving the highest AIC weights, and provide recommendations related to the set of models included in the analyses that reduce these rates by half. Finally, we demonstrate that trees including clades following different dependent‐drivers affect RPANDA analyses by producing different outcomes, ranging from partially correct models to completely misleading results. We provide recommendations for the implementation of both programs.