ACDC: Analysis of Congruent Diversification Classes

Diversification rates inferred from phylogenies are not identifiable. There are infinitely many combinations of speciation and extinction rate functions that have the exact same likelihood score for a given phylogeny, building a congruence class. The specific shape and characteristics of such congruence classes have not yet been studied. Whether speciation and extinction rate functions within a congruence class share common features is also not known. Instead of striving to make the diversification rates identifiable, we can embrace their inherent non-identifiable nature. We use two different approaches to explore a congruence class: (i) testing of specific alternative hypotheses, and (ii) randomly sampling alternative rate function within the congruence class. Our methods are implemented in the open-source R package ACDC (https://github.com/afmagee/ACDC). ACDC provides a flexible approach to explore the congruence class and provides summaries of rate functions within a congruence class. The summaries can highlight common trends, i.e. increasing, flat or decreasing rates. Although there are infinitely many equally likely diversification rate functions, these can share common features. ACDC can be used to assess if diversification rate patterns are robust despite non-identifiability. In our example, we clearly identify three phases of diversification rate changes that are common among all models in the congruence class. Thus, congruence classes are not necessarily a problem for studying historical patterns of biodiversity from phylogenies.

Maternal investment evolves with larger body size and higher diversification rate in sharks and rays

Across vertebrates, live-bearing has evolved at least 150 times from the ancestral state of egg-laying into a diverse array of forms and degrees of prepartum maternal investment. A key question is how this diversity of reproductive modes arose and whether reproductive diversification underlies species diversification? To test these questions, we evaluate the most basal jawed vertebrates, Chondrichthyans, which have one of the greatest ranges of reproductive and ecological diversity among vertebrates. We reconstructed the sequence of reproductive mode evolution across a time-calibrated molecular phylogeny of 610 chondrichthyans. We find that egg-laying is ancestral, and that live-bearing evolved at least seven times. Matrotrophy (i.e. additional maternal contributions) evolved at least 15 times, with evidence of one reversal. In sharks, transitions to live-bearing and matrotrophy are more prevalent in larger-bodied species in the tropics. Further, the evolution of live-bearing is associated with a near-doubling of the diversification rate, but, there is only a small increase in diversification associated with the appearance of matrotrophy. The chondrichthyan diversification and radiation, particularly throughout the shallow tropical shelf seas and oceanic pelagic habitats, appears to be associated with the evolution of live-bearing and the proliferation of a wide range of maternal investment in their developing offspring.

Floral evolution and pollinator diversification in Hedychium J.Koenig (Zingiberaceae): one of Mr. Darwin’s tropical fantasies

ABSTRACTPREMISEHedychium J.Koenig (ginger lilies: Zingiberaceae) is endemic to the Indo-Malayan Realm (IMR) and is known for its fragrant flowers. Two different pollination syndromes characterize the genus: diurnal or bird pollination and nocturnal or moth pollination systems. To date, no attempt has been undertaken to understand the evolution of floral traits in this genus.METHODSWe estimated ancestral character-states, phylogenetic signals, and character correlations for thirteen discrete and eight continuous floral traits representing 75% species diversity of Hedychium. Diversification rate estimation analyses were also employed to understand trait-dependent diversification in the genus.RESULTSInflorescence structure, cincinnus capacity, and curvature of floral tubes revealed strong phylogenetic dependence, whereas number of open flowers per inflorescence per day, color of the labellum, and exertion of the stigma characterized higher ecological effects. Diversification rate estimations suggested that the labellum width, floral tube length, and labellum color played a major role in the evolutionary diversification of Hedychium.CONCLUSIONSWe identified bract type and cincinnus capacity as synapomorphies for Hedychium, while the island-specific clade III was characterized by slender cylindrical inflorescence, coiling of floral tubes, and longer bract to calyx ratio. The circum-Himalayan clade IV is the most speciose, derived, and with most variable floral traits. Although floral color and size lacked any association with pollinator-specific traits (moth and bird pollination), pale colored flowers were most common in the early diverging clades (clade I, II-el., and II-de.), indicating their ancestral nature, when compared to brightly colored flowers.

Fossils Do Not Substantially Improve, and May Even Harm, Estimates of Diversification Rate Heterogeneity

There is a prevailing view that the inclusion of fossil data could remedy identifiability issues related to models of diversification, by drastically reducing the number of congruent models. The fossilized birth-death (FBD) model is an appealing way of directly incorporating fossil information when estimating diversification rates. Here we explore the benefits of including fossils by implementing and then testing two-types of FBD models in more complex likelihood-based models that assume multiple rate classes across the tree. We also assess the impact of severely undersampling, and even not including fossils that represent samples of lineages that also had sampled descendants (i.e., k-type fossils), as well as converting a fossil set to represent stratigraphic ranges. Under various simulation scenarios, including a scenario that exists far outside the set of models we evaluated, including fossils rarely outperforms analyses that exclude them altogether. At best, the inclusion of fossils improves precision but does not influence bias. We also found that severely undercounting the number of k-type fossils produces highly inflated rates of turnover and extinction fraction. Similarly, we found that converting the fossil set to stratigraphic ranges results in turnover rates and extinction fraction estimates that are generally underestimated. While fossils remain essential for understanding diversification through time, in the specific case of understanding diversification given an existing, largely modern tree, they are not especially beneficial.

Fruit colour and range size interact to influence diversification

Aim: Different fruit colours are associated with dispersal by different frugivores, largely based on colour vision type. Frugivore mobility affects overall range size for the plant being dispersed. Here we determine the interaction between different fruit colours, range sizes, and diversification rates by testing two hypotheses: That (1) fruit colours attractive to birds have larger range sizes due to their higher dispersal ability, and that (2) different frugivore disperser groups, bird or mammal, leads to different diversification rate at different range size, where intermediate range size leads to the highest diversification rate. Location: Global. Time period: Contemporary (or present). Major taxa studied: Palms (Arecaceae). Methods: Using model selection, we identified three groups of colours with similar diversification rate and likely disperser. Range sizes were estimated and categorized species as small, intermediate, or large-ranged. For model selection and to determine the relationship beween fruit color, range size and diversification rate we used Multi-State Speciation and Extinction (MuSSE) models. Results: Species with intermediate range size had the highest net diversification for all three fruit colour groups. Bird-dispersed palms more likely diversified at small than at large range size while mammal-dispersed palms more likely diversified at larger range size than small. Fruit colours associated with mammal dispersal had more large-ranged species than colours associated with bird dispersal. Main conclusions: The associated between intermediate range size and higher diversification rate indicates that spatial factors that affect diversification at small and large range sizes result in higher diversification at intermediate ranges. We find striking differences in diversification rate within each range size category between fruit color groups. This suggests that the relationship between diversification rate and range size depends on the specific frugivorous dispersers and their dispersal patterns. This study reveals how fruit traits alter dispersal patterns and how that, in turn, influences diversification.

The Evolution of Nest Site Specialization and its Macroevolutionary Consequences in Passerine Birds

A long-standing hypothesis in evolutionary biology is that the evolution of resource specialization can lead to an evolutionary dead end, where specialists have low diversification rates and limited ability to evolve into generalists. However, in recent years, advances in comparative methods investigating trait-based differences associated with diversification have enabled more robust tests of this idea and have found mixed support. Here we test the evolutionary dead end hypothesis by estimating net diversification rate differences associated with nest site specialization among 3,224 species of passerine birds. In particular, we test whether the adoption of hole-nesting, a nest site specialization that decreases predation, results in reduced diversification rates relative to nesting outside of holes. Further, we examine whether evolutionary transitions to the specialist hole-nesting state have been more frequent than transitions out of hole-nesting. Using diversification models that accounted for background rate heterogeneity and different extinction rate scenarios, we found that hole-nesting specialization was not associated with diversification rate differences. Furthermore, contrary to the assumption that specialists rarely evolve into generalists, we found that transitions out of hole-nesting occur more frequently than transitions into hole-nesting. These results suggest that interspecific competition may limit adoption of hole-nesting, but that such competition does not result in limited diversification of hole-nesters. In conjunction with other recent studies using robust comparative methods, our results add to growing evidence that evolutionary dead ends are not a typical outcome of resource specialization.

Ciliates as Symbionts

Although many ciliates are free-living, more than 140 families of ciliates (Alveolata, Ciliophora) include symbiotic species of animals. Symbiosis, defined as an interaction between two species, is analyzed in this chapter to show a wide diversity of symbiotic systems in ciliates (epibiosis, commensalism, mutualism, and parasitism), providing some data about ciliate strategies showing their success as symbionts. Some species are free-living as well symbionts, facultative symbionts, and obligate symbionts. Analysis of reconstructions of ancestral state evidence that the parasitism arose numerous times and independently among the lineages of ciliates. At least three evolutionary routes can be traced: (1) transition from free-living to mutualism and parasitism, (2) transition from free-living to parasitism, and (3) regression from parasitism to free-living. The evolution of the symbiosis in ciliates demonstrates a higher diversification rate concerning free-living ciliates. The analysis of the evolution of the life cycles complexity, exploring molecular data of the phases of the ciliate cycle in their hosts is also essential. We propose new approaches for an integrative study of symbiotic ciliates.

Asynchronous rates of lineage, phenotype, and niche diversification in a continental-scale adaptive radiation

Rapidly diversifying clades are central to the study of diversification dynamics. This central importance is perhaps most apparent when rapid evolution occurs across several axes of diversification (e.g., lineage, phenotype, and niche); such clades facilitate investigations into the interplay between adaptive and non-adaptive diversification mechanisms. Yet, empirical evidence from rapidly evolving clades remains unclear about the relationships, if any, across diversification axes. This is especially apparent regarding the timing of diversification rate shifts. We address this knowledge gap through comparisons of the rate and timing of lineage, phenotypic, and niche diversification in Penstemon, a rapidly-evolving angiosperm genus. We find that diversification rate shifts in Penstemon are asynchronous; while we identify a burst and subsequent slowdown in lineage diversification rate ~2.0-2.5 MYA, shifts in phenotypic and niche diversification rates either lagged behind temporally or did not occur at all. We posit that this asynchronicity in diversification rate shifts is the result of initial niche-neutral diversification followed by adaptive, density-dependent processes. Our findings contribute to a growing body of evidence that asynchronous shifts in diversification rates may be common and question the applicability of expectations for diversification dynamics across disparate empirical systems.

Phylogenomic and ecological analyses reveal the spatiotemporal evolution of global pines

How coniferous forests evolved in the Northern Hemisphere remains largely unknown. Unlike most groups of organisms that generally follow a latitudinal diversity gradient, most conifer species in the Northern Hemisphere are distributed in mountainous areas at middle latitudes. It is of great interest to know whether the midlatitude region has been an evolutionary cradle or museum for conifers and how evolutionary and ecological factors have driven their spatiotemporal evolution. Here, we investigated the macroevolution of Pinus, the largest conifer genus and characteristic of northern temperate coniferous forests, based on nearly complete species sampling. Using 1,662 genes from transcriptome sequences, we reconstructed a robust species phylogeny and reestimated divergence times of global pines. We found that ∼90% of extant pine species originated in the Miocene in sharp contrast to the ancient origin of Pinus, indicating a Neogene rediversification. Surprisingly, species at middle latitudes are much older than those at other latitudes. This finding, coupled with net diversification rate analysis, indicates that the midlatitude region has provided an evolutionary museum for global pines. Analyses of 31 environmental variables, together with a comparison of evolutionary rates of niche and phenotypic traits with a net diversification rate, found that topography played a primary role in pine diversification, and the aridity index was decisive for the niche rate shift. Moreover, fire has forced diversification and adaptive evolution of Pinus. Our study highlights the importance of integrating phylogenomic and ecological approaches to address evolution of biological groups at the global scale.

Ecological and evolutionary constraints on regional avifauna of passerines in China

Strong correlations between species diversity and climate have been widely observed, but the mechanism underlying this relationship is unclear. Here, we explored the causes of the richness–climate relationships among passerine birds in China by integrating tropical conservatism and diversification rate hypotheses using path models. We found that assemblages with higher species richness southwest of the Salween–Mekong–Pearl River Divide are phylogenetically overdispersed and have shorter mean root distances (MRDs), while species-rich regions northeast of this divide (e.g., north Hengduan Mountains–south Qinling Mountains) are phylogenetically clustered and have longer MRDs. The results of the path analyses showed that the direct effect of climatic factors on species richness was stronger than their indirect effects on species richness via phylogenetic relatedness, indicating that neither tropical conservatism nor diversification rate hypotheses can well explain the richness–climate relationship among passerines in China. However, when path analyses were conducted within subregions separately, we found that the tropical conservatism hypothesis was well supported in the southwestern Salween–Mekong–Pearl River Divide, while the diversification rate hypothesis could explain the richness–climate relationship well in the northeastern divide. We conclude that the diversity patterns of passerines in different subregions of the Eastern Himalayas-Mountains of Southwest China may be shaped by different evolutionary processes related to geological and climatic histories, which explains why the tropical conservatism or diversification rate hypothesis alone cannot fully explain the richness–climate relationships.