Decrease In Diversification Rate Research Articles

Macroevolution of the plant-hummingbird pollination system.

Plant-hummingbird interactions are considered a classic example of coevolution, a process in which mutually dependent species influence each other's evolution. Plants depend on hummingbirds for pollination, whereas hummingbirds rely on nectar for food. As a step towards understanding coevolution, this review focuses on the macroevolutionary consequences of plant-hummingbird interactions, a relatively underexplored area in the current literature. We synthesize prior studies, illustrating the origins and dynamics of hummingbird pollination across different angiosperm clades previously pollinated by insects (mostly bees), bats, and passerine birds. In some cases, the crown age of hummingbirds pre-dates the plants they pollinate. In other cases, plant groups transitioned to hummingbird pollination early in the establishment of this bird group in the Americas, with the build-up of both diversities coinciding temporally, and hence suggesting co-diversification. Determining what triggers shifts to and away from hummingbird pollination remains a major open challenge. The impact of hummingbirds on plant diversification is complex, with many tropical plant lineages experiencing increased diversification after acquiring flowers that attract hummingbirds, and others experiencing no change or even a decrease in diversification rates. This mixed evidence suggests that other extrinsic or intrinsic factors, such as local climate and isolation, are important covariables driving the diversification of plants adapted to hummingbird pollination. To guide future studies, we discuss the mechanisms and contexts under which hummingbirds, as a clade and as individual species (e.g. traits, foraging behaviour, degree of specialization), could influence plant evolution. We conclude by commenting on how macroevolutionary signals of the mutualism could relate to coevolution, highlighting the unbalanced focus on the plant side of the interaction, and advocating for the use of species-level interaction data in macroevolutionary studies.

Irreversible habitat specialization does not constrain diversification in hypersaline water beetles.

Specialization to extreme environments is often considered an evolutionary dead-end, leading to irreversible adaptations and reduced evolvability. There is, however, mixed evidence for this macroevolutionary pattern, and limited data from speciose lineages. Here, we tested the effect of habitat specialization to hypersaline waters in the diversification rates of aquatic beetles of the genus Ochthebius (Coleoptera, Hydraenidae), using a molecular phylogeny with more than 50% of the 546 recognized species, including representatives of all but one of the nine recognized subgenera and 17 species groups. Phylogenies were built combining mitochondrial and nuclear genes, with the addition of 42 mitochondrial genomes. Using Bayesian methods of character reconstruction, we show that hypersaline tolerance is an irreversible ecological specialization that arose multiple times. Two lineages of Ochthebius experienced a significant increase in diversification rates, one of them inhabiting hypersaline waters, but there was no overall correlation with habitat or any significant decrease in diversification rates despite the irreversibility of hypersaline tolerance. Our study tested for the first time the impact of hypersaline habitat specialization on diversification rates, finding no support for it to be an evolutionary dead-end. On the contrary, multiple and ancient lineages fully adapted to these extreme osmotic conditions have persisted and diversified over a long evolutionary timescale.

Extinction pulse at Eocene-Oligocene boundary drives diversification dynamics of two Australian temperate floras.

The diversification dynamics of the Australian temperate flora remains poorly understood. Here, we investigate whether differences in plant richness in the southwest Australian (SWA) biodiversity hotspot and southeast Australian (SEA) regions of the Australian continent can be attributed to higher net diversification, more time for species accumulation, or both. We assembled dated molecular phylogenies for the 21 most species-rich flowering plant families found across mesic temperate Australia, encompassing both SWA and SEA regions, and applied a series of diversification models to investigate responses across different groups and timescales. We show that the high richness in SWA can be attributed to a higher net rate of lineage diversification and more time for species accumulation. Different pulses of diversification were retrieved in each region. A decrease in diversification rate across major flowering plant lineages at the Eocene-Oligocene boundary (ca 34 Ma) was witnessed in SEA but not in SWA. Our study demonstrates the importance of historical diversification pulses and differential responses to global events as drivers of present-day diversity. More broadly, we show that diversity within the SWA biodiversity hotspot is not only the result of recent radiations, but also reflects older events over the history of this planet.

Biogeography and diversification dynamics of the African woodpeckers

The dynamics of species accumulation of African terrestrial vertebrates over time remains underexplored in comparison with those in the New World, despite Africa hosting about 25% of the world’s avian diversity. This lack of knowledge hampers our understanding of the fundamental processes that drive biodiversity and the dynamics of speciation. To begin to address this gap, we reconstructed species-level phylogenies of two unrelated clades of African woodpeckers (12 species of Geocolaptes/Campethera and 13 species of Chloropicus/Mesopicos/Dendropicos/Ipophilus) that diverged from their closest Indo-Malayan relatives at similar times. Our results demonstrate that the current taxonomy is misleading: three (Campethera, Dendropicos and Mesopicos) out of four polytpic genera/subgenera are not monophyletic. Our results also show that current estimates of diversity at the species level are significantly understated, as up to 18 species for the ‘Campethera clade’ and 19 for the ‘Dendropicos clade’ could be recognized. The first splits within both clades involve species that are largely restricted to the Guineo-Congolian biogeographic regions, followed by later adaptations to particular habitats (forest versus savannah) and colonization of other regions (e.g. Southern Africa), each of which occurred multiple times in both clades. Assuming a conservative species delimitation scheme, our results indicate that diversification rates are decreasing through time for both clades. Applying a more extreme species recognition scheme (18 and 19 species for the Campethera and Dendropicos clades, respectively), our results support a decrease in diversification rates only for the Dendropicos clade and thus underline the importance of the number of species included in our diversification analyses. Greater ecological diversity of the Campethera clade where multiple species exhibit either an arboreal or terrestrial foraging strategy might explain the constant diversification rates through time we found under the eighteen species scheme.

The explosive radiation of Cheirolophus (Asteraceae, Cardueae) in Macaronesia.

BackgroundConsidered a biodiversity hotspot, the Canary Islands have been the key subjects of numerous evolutionary studies concerning a large variety of organisms. The genus Cheirolophus (Asteraceae) represents one of the largest plant radiations in the Canarian archipelago. In contrast, only a few species occur in the Mediterranean region, the putative ancestral area of the genus. Here, our main aim was to reconstruct the phylogenetic and biogeographic history of Cheirolophus with special focus on explaining the origin of the large Canarian radiation.ResultsWe found significant incongruence in phylogenetic relationships between nuclear and plastid markers. Each dataset provided resolution at different levels in Cheirolophus: the nuclear markers resolved the backbone of the phylogeny while the plastid data provided better resolution within the Canarian clade. The origin of Cheirolophus was dated in the Mid-Late Miocene, followed by rapid diversification into the three main Mediterranean lineages and the Macaronesian clade. A decrease in diversification rates was inferred at the end of the Miocene, with a new increase in the Late Pliocene concurrent with the onset of the Mediterranean climate. Diversification within the Macaronesian clade started in the Early-Mid Pleistocene, with unusually high speciation rates giving rise to the extant insular diversity.ConclusionsClimate-driven diversification likely explains the early evolutionary history of Cheirolophus in the Mediterranean region. It appears that the exceptionally high diversification rate in the Canarian clade was mainly driven by allopatric speciation (including intra- and interisland diversification). Several intrinsic (e.g. breeding system, polyploid origin, seed dispersal syndrome) and extrinsic (e.g. fragmented landscape, isolated habitats, climatic and geological changes) factors probably contributed to the progressive differentiation of populations resulting in numerous microendemisms. Finally, hybridization events and emerging ecological adaptation may have also reinforced the diversification process.

Diversification patterns and processes of wingless endemic insects in the Mediterranean Basin: historical biogeography of the genusBlaps(Coleoptera: Tenebrionidae)

Aim The 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. Location Mediterranean Basin. Methods We 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. Results The 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 conclusions Our 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.

Evolution of microgastropods (Ellobioidea, Carychiidae): integrating taxonomic, phylogenetic and evolutionary hypotheses

BackgroundCurrent biodiversity patterns are considered largely the result of past climatic and tectonic changes. In an integrative approach, we combine taxonomic and phylogenetic hypotheses to analyze temporal and geographic diversification of epigean (Carychium) and subterranean (Zospeum) evolutionary lineages in Carychiidae (Eupulmonata, Ellobioidea). We explicitly test three hypotheses: 1) morphospecies encompass unrecognized evolutionary lineages, 2) limited dispersal results in a close genetic relationship of geographical proximally distributed taxa and 3) major climatic and tectonic events had an impact on lineage diversification within Carychiidae.ResultsInitial morphospecies assignments were investigated by different molecular delimitation approaches (threshold, ABGD, GMYC and SP). Despite a conservative delimitation strategy, carychiid morphospecies comprise a great number of unrecognized evolutionary lineages. We attribute this phenomenon to historic underestimation of morphological stasis and phenotypic variability amongst lineages. The first molecular phylogenetic hypothesis for the Carychiidae (based on COI, 16S and H3) reveals Carychium and Zospeum to be reciprocally monophyletic. Geographical proximally distributed lineages are often closely related. The temporal diversification of Carychiidae is best described by a constant rate model of diversification. The evolution of Carychiidae is characterized by relatively few (long distance) colonization events. We find support for an Asian origin of Carychium. Zospeum may have arrived in Europe before extant members of Carychium. Distantly related Carychium clades inhabit a wide spectrum of the available bioclimatic niche and demonstrate considerable niche overlap.ConclusionsCarychiid taxonomy is in dire need of revision. An inferred wide distribution and variable phenotype suggest underestimated diversity in Zospeum. Several Carychium morphospecies are results of past taxonomic lumping. By collecting populations at their type locality, molecular investigations are able to link historic morphospecies assignments to their respective evolutionary lineage. We propose that rare founder populations initially colonized a continent or cave system. Subsequent passive dispersal into adjacent areas led to in situ pan-continental or mountain range diversifications. Major environmental changes did not influence carychiid diversification. However, certain molecular delimitation methods indicated a recent decrease in diversification rate. We attribute this decrease to protracted speciation.

Diversification of subgenus Calathus (Coleoptera: Carabidae) in the Mediterranean region – glacial refugia and taxon pulses

AbstractAim 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.

Community assembly and diversification in Indo-Pacific coral reef fishes.

Theories of species coexistence have played a central role in ecology and evolutionary studies of the origin and maintenance of biodiversity in highly diverse communities. The concept of niche and associated theories predict that competition for available ecological space leads to a ceiling in species richness that influences further diversification patterns. By contrast, the neutral theory supports that speciation is stochastic and diversity independent. We examined the phylogenetic community structure and diversification rates in three families and 14 sites within coral reef fish communities from the Indian and Pacific oceans. Using the phylogenetic relationships among 157 species estimated with 2300 bp of mitochondrial DNA, we tested predictions in terms of species coexistence from the neutral and niche theories. At the regional scale, our findings suggest that phylogenetic community structure shifts during community assembly to a pattern of dispersion as a consequence of allopatric speciation in recent times but overall, variations in diversification rates did not relate with sea level changes. At the local scale, the phylogenetic community structure is consistent with a neutral model of community assembly since no departure from a random sorting of species was observed. The present results support a neutral model of community assembly as a consequence of the stochastic and unpredictable nature of coral reefs favoring generalist and sedentary species competing for living space rather than trophic resources. As a consequence, the observed decrease in diversification rates may be seen as the result of a limited supply of living space as expected in a finite island model.

The Molecular Phylogenetic Signature of Clades in Decline

Molecular phylogenies have been used to study the diversification of many clades. However, current methods for inferring diversification dynamics from molecular phylogenies ignore the possibility that clades may be decreasing in diversity, despite the fact that the fossil record shows this to be the case for many groups. Here we investigate the molecular phylogenetic signature of decreasing diversity using the most widely used statistic for inferring diversity dynamics from molecular phylogenies, the γ statistic. We show that if a clade is in decline its molecular phylogeny may show evidence of the decrease in the diversification rate that occurred between its diversification and decline phases. The ability to detect the change in diversification rate depends largely on the ratio of the speciation rates of the diversification and decline phases, the higher the ratio the stronger the signal of the change in diversification rate. Consequently, molecular phylogenies of clades in relative rapid decline do not carry a signature of their decreasing diversification. Further, the signal of the change in diversification rate, if present, declines as the diversity drop. Unfortunately, the molecular signature of clades in decline is the same as the signature produced by diversity dependent diversification. Given this similarity, and the inability of current methods to detect declining diversity, it is likely that some of the extant clades that show a decrease in diversification rate, currently interpreted as evidence for diversity dependent diversification, are in fact in decline. Unless methods can be developed that can discriminate between the different modes of diversification, specifically diversity dependent diversification and declining diversity, we will need the fossil record, or data from some other source, to distinguish between these very different diversity trajectories.

Interpreting the γ Statistic in Phylogenetic Diversification Rate Studies: A Rate Decrease Does Not Necessarily Indicate an Early Burst

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.

Phylogenetic diversification patterns and divergence times in ground beetles (Coleoptera: Carabidae: Harpalinae).

BackgroundHarpalinae is a species rich clade of carabid beetles with many unusual morphological forms and ecological interactions. How this diversity evolved has been difficult to reconstruct, perhaps because harpalines underwent a rapid burst of diversification early in their evolutionary history. Here we investigate the tempo of evolution in harpalines using molecular divergence dating techniques and explore the rates of lineage accumulation in harpalines and their sister group.ResultsAccording to molecular divergence date estimates, harpalines originated in the mid Cretaceous but did not diversify extensively until the late Cretaceous or early Paleogene about 32 million years after their origin. In a relatively small window of time, harpalines underwent rapid speciation. Harpalines have a relative high net diversification rate and increased cladogenesis in some regions of the clade. We did not see a significant decrease in diversification rate through time in the MCCR test, but a model of diversification with two shift points to lower diversification rates fit the harpaline lineage accumulation through time the best.ConclusionsOur results indicate harpalines are significantly more diverse and have higher diversification than their sistergroup. Instead of an immediate burst of explosive diversification, harpalines may have had a long "fuse" before major lineages diversified during the early Paleogene when other taxa such as mammals, birds, and some flowering plants were also rapidly diversifying.

EXTINCTION DURING EVOLUTIONARY RADIATIONS: RECONCILING THE FOSSIL RECORD WITH MOLECULAR PHYLOGENIES

Recent application of time-varying birth-death models to molecular phylogenies suggests that a decreasing diversification rate can only be observed if there was a decreasing speciation rate coupled with extremely low or no extinction. However, from a paleontological perspective, zero extinction rates during evolutionary radiations seem unlikely. Here, with a more comprehensive set of computer simulations, we show that substantial extinction can occur without erasing the signal of decreasing diversification rate in a molecular phylogeny. We also find, in agreement with the previous work, that a decrease in diversification rate cannot be observed in a molecular phylogeny with an increasing extinction rate alone. Further, we find that the ability to observe decreasing diversification rates in molecular phylogenies is controlled (in part) by the ratio of the initial speciation rate (Lambda) to the extinction rate (Mu) at equilibrium (the LiMe ratio), and not by their absolute values. Here we show in principle, how estimates of initial speciation rates may be calculated using both the fossil record and the shape of lineage through time plots derived from molecular phylogenies. This is important because the fossil record provides more reliable estimates of equilibrium extinction rates than initial speciation rates.

Diversification of myco-heterotrophic angiosperms: evidence from Burmanniaceae.

BackgroundMyco-heterotrophy evolved independently several times during angiosperm evolution. Although many species of myco-heterotrophic plants are highly endemic and long-distance dispersal seems unlikely, some genera are widely dispersed and have pantropical distributions, often with large disjunctions. Traditionally this has been interpreted as evidence for an old age of these taxa. However, due to their scarcity and highly reduced plastid genomes our understanding about the evolutionary histories of the angiosperm myco-heterotrophic groups is poor.ResultsWe provide a hypothesis for the diversification of the myco-heterotrophic family Burmanniaceae. Phylogenetic inference, combined with biogeographical analyses, molecular divergence time estimates, and diversification analyses suggest that Burmanniaceae originated in West Gondwana and started to diversify during the Late Cretaceous. Diversification and migration of the species-rich pantropical genera Burmannia and Gymnosiphon display congruent patterns. Diversification began during the Eocene, when global temperatures peaked and tropical forests occurred at low latitudes. Simultaneous migration from the New to the Old World in Burmannia and Gymnosiphon occurred via boreotropical migration routes. Subsequent Oligocene cooling and breakup of boreotropical flora ended New-Old World migration and caused a gradual decrease in diversification rate in Burmanniaceae.ConclusionOur results indicate that extant diversity and pantropical distribution of myco-heterotrophic Burmanniaceae is the result of diversification and boreotropical migration during the Eocene when tropical rain forest expanded dramatically.

The Temporal Course of Quaternary Diversification in the European High Mountain EndemicPrimulasect.Auricula(Primulaceae)

Primula sect. Auricula is one of only a few endemics of the European high mountains with a comparatively large number of species. We explored the section’s geographical origin, time of origin, and temporal course of diversification via parsimony, genetic distance, and lineages‐through‐time analyses based on the internal transcribed spacer (ITS) regions of nuclear ribosomal DNA. The taxa analyzed included 52 individuals representing all 25 species of the section, representatives of seven other European, Asian, and/or North American sections of the genus, and two species of Douglasia. We present evidence that sect. Auricula likely originated from an Asian ancestor at the end of the Late Tertiary, followed by its primary diversification into an “eastern” and “western” lineage at the Plio‐/Pleistocene boundary. Comparison with a constant rates null model of stochastic diversification‐extinction (birth‐death) demonstrates that diversification has proceeded nonrandomly through Quaternary times in both lineages. They display a pulse of speciation events occurring soon after their origin and relatively few such events occurring since. This pattern contrasts with the predictions of the Late Pleistocene origins hypothesis and implies unpredictability of the evolutionary response of sect. Auricula to the recurrent abiotic conditions of the Quaternary glacial‐interglacial cycles. We conclude that it is not necessary to invoke an increase in extinction rate. Rather, the observed slowdown of interspecific (and intraspecific) diversification in sect. Auricula toward the present likely results from a decrease in diversification rate due to ecological and/or geographical space‐filling processes.