Dissecting the Complexity of Early Heart Progenitor Cells

Early heart development depends on the coordinated participation of heterogeneous cellsources. As pioneer work from Adriana C. Gittenberger-de Groot demonstrated, characterizing thesedistinct cell sources helps us to understand congenital heart defects. Despite decades of researchon the segregation of lineages that form the primitive heart tube, we are far from understanding itsfull complexity. Currently, single-cell approaches are providing an unprecedented level of detail oncellular heterogeneity, offering new opportunities to decipher its functional role. In this review, wewill focus on three key aspects of early heart morphogenesis: First, the segregation of myocardial andendocardial lineages, which yields an early lineage diversification in cardiac development; second,the signaling cues driving differentiation in these progenitor cells; and third, the transcriptionalheterogeneity of cardiomyocyte progenitors of the primitive heart tube. Finally, we discuss howsingle-cell transcriptomics and epigenomics, together with live imaging and functional analyses, willlikely transform the way we delve into the complexity of cardiac development and its links withcongenital defects.

Landscape dynamics promoted the evolution of mega-diversity in South American freshwater fishes

Landscape dynamics and river network rearrangements are widely thought to shape the diversity of Neotropical freshwater fishes, the most species-rich continental vertebrate fauna on Earth. Yet the effects of hydrogeographic changes on fish dispersal and diversification remain poorly understood. Here we integrate an unprecedented occurrence dataset of 4,967 South American freshwater fish species with a species-dense phylogeny to track the evolutionary processes associated with hydrogeographic events over 100 Ma. Net lineage diversification was heterogeneous through time, across space, and among clades. Three abrupt shifts in diversification rates occurred during the Paleogene (between 63 and 23 Ma) in association with major landscape evolution events, and net diversification accelerated from the Miocene to the Recent (c. 20 - 0 Ma). The Western Amazon exhibited the highest rates of in situ diversification and was also the most important source of species dispersing to other regions. All regional biotic interchanges were associated with documented hydrogeographic events and the formation of biogeographic corridors, including Early Miocene (c. 20 Ma) uplift of the Serra do Mar, and Late Miocene (c. 10 Ma) uplift of the Northern Andes and formation of the modern transcontinental Amazon River. Reciprocal mass dispersal of fishes between the Western and Eastern Amazon coincided with this phase of Andean uplift. The Western Amazon has the highest contemporary levels of species richness and phylogenetic endemism. Our results support the hypothesis that landscape dynamics were constrained by the history of drainage basin connections, strongly affecting the assembly and diversification of basin-wide fish faunas.

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.

A genomics dissection of Kenya’s COVID-19 waves: temporal lineage replacements and dominance of imported variants of concern

Kenya’s COVID-19 epidemic was slow to peak. It was seeded early in March 2020, and did not peak until late-July 2020 (wave 1), mid-November 2020 (wave 2) and late-March 2021 (wave 3). Here we present SARS-CoV-2 lineages associated with the three COVID-19 waves through analysis of 483 genomes, which included 167 Alpha (B.1.1.7), 57 Delta (B.1.617.2) and 12 Beta (B.1.351) variants of concerns (VOC) that dominated the third wave. In total, 35 lineages were identified. The early European lineages B.1 and B.1.1 were the first to be seeded in Kenya. The B.1 lineage continued to expand and remained the most dominant lineage accounting for 55.8% and 56.3% in waves 1 and 2 respectively. The alpha (B.1.1.7), delta (B.1.167.2) and beta (B.1.351) VOCs dominated in wave 3 at 59.0%, 20.1% and 4.2% respectively. Eventually, the delta variant took over at the tail end of wave 3 and at the time of going to press, it had become the major lineage in the whole country. Phylogenetic analysis suggested multiple introductions of variants from outside Kenya especially during the first and third wave. Phylogeny also highlighted local lineage diversification as local transmission events supervened. The data highlights the importance of genome surveillance in determining circulating variants to aid in public health interventions.

Causes and Consequences of Apparent Timescaling Across All Estimated Evolutionary Rates

Evolutionary rates play a central role in connecting micro- and macroevolution. All evolutionary rate estimates, including rates of molecular evolution, trait evolution, and lineage diversification, share a similar scaling pattern with time: The highest rates are those measured over the shortest time interval. This creates a disconnect between micro- and macroevolution, although the pattern is the opposite of what some might expect: Patterns of change over short timescales predict that evolution has tremendous potential to create variation and that potential is barely tapped by macroevolution. In this review, we discuss this shared scaling pattern across evolutionary rates. We break down possible explanations for scaling into two categories, estimation error and model misspecification, and discuss how both apply to each type of rate. We also discuss the consequences of this ubiquitous pattern, which can lead to unexpected results when comparing rates over different timescales. Finally, after addressing purely statistical concerns, we explore a few possibilities for a shared unifying explanation across the three types of rates that results from a failure to fully understand and account for how biological processes scale over time. Expected final online publication date for the Annual Review of Ecology, Evolution, and Systematics, Volume 52 is November 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

Snakes on an African plain: the radiation of Crotaphopeltis and Philothamnus into open habitat (Serpentes: Colubridae)

Background The African continent is comprised of several different biomes, although savanna is the most prevalent. The current heterogeneous landscape was formed through long-term vegetation shifts as a result of the global cooling trend since the Oligocene epoch. The overwhelming trend was a shift from primarily forest, to primarily savanna. As such, faunal groups that emerged during the Paleogene/Neogene period and have species distributed in both forest and savanna habitat should show a genetic signature of the possible evolutionary impact of these biome developments. Crotaphopeltis and Philothamnus (Colubridae) are excellent taxa to investigate the evolutionary impact of these biome developments on widespread African colubrid snakes, and whether timing and patterns of radiation are synchronous with biome reorganisation. Methods A phylogenetic framework was used to investigate timing of lineage diversification. Phylogenetic analysis included both genera as well as other Colubridae to construct a temporal framework in order to estimate radiation times for Crotaphopeltis and Philothamnus. Lineage diversification was estimated in Bayesian Evolutionary Analysis Sampling Trees (BEAST), using two mitochondrial markers (cyt–b, ND4), one nuclear marker (c–mos), and incorporating one fossil and two biogeographical calibration points. Vegetation layers were used to classify and confirm species association with broad biome types (‘closed’ = forest, ‘open’ = savanna/other), and the ancestral habitat state for each genus was estimated. Results Philothamnus showed an ancestral state of closed habitat, but the ancestral habitat type for Crotaphopeltis was equivocal. Both genera showed similar timing of lineage diversification diverging from their sister genera during the Oligocene/Miocene transition (ca. 25 Mya), with subsequent species radiation in the Mid-Miocene. Philothamnus appeared to have undergone allopatric speciation during Mid-Miocene forest fragmentation. Habitat generalist and open habitat specialist species emerged as savanna became more prevalent, while at least two forest associated lineages within Crotaphopeltis moved into Afromontane forest habitat secondarily and independently. Discussion With similar diversification times, but contrasting ancestral habitat reconstructions, we show that these genera have responded very differently to the same broad biome shifts. Differences in biogeographical patterns for the two African colubrid genera is likely an effect of distinct life-history traits, such as the arboreous habits of Philothamnus compared to the terrestrial lifestyle of Crotaphopeltis.

Prolonged morphological expansion of spiny-rayed fishes following the end-Cretaceous

Spiny-rayed fishes (Acanthomorpha) dominate modern marine habitats and comprise more than a quarter of all living vertebrate species1-3. It is believed that this dominance resulted from explosive lineage and phenotypic diversification coincident with the Cretaceous-Paleogene (K-Pg) mass-extinction event4. It remains unclear, however, if living acanthomorph diversity is the result of a punctuated burst or gradual accumulation of diversity following the K-Pg. We assess these hypotheses with a time-calibrated phylogeny inferred using ultraconserved elements from a sampling of species that represent over 91% of all acanthomorph families, as well as an extensive body shape dataset of extant species. Our results indicate that several million years after the end-Cretaceous, acanthomorphs underwent a prolonged and significant expansion of morphological disparity primarily driven by changes in body elongation, and that acanthomorph lineages containing the bulk of the living species diversity originated throughout the Cenozoic. These acanthomorph lineages radiated into distinct regions of morphospace and retained their iconic phenotypes, including a large group of laterally compressed reef fishes, fast-swimming open-ocean predators, bottom-dwelling flatfishes, seahorses, and pufferfishes. The evolutionary success of spiny-rayed fishes is the culmination of a post K-Pg adaptive radiation in which rates of lineage diversification were decoupled from periods of high phenotypic disparity.

Mistreating birth-death models as priors in phylogenetic analysis compromises our ability to compare models

Time-calibrated phylogenetic trees are fundamental to a wide range of evolutionary studies. Typically, these trees are inferred in a Bayesian framework, with the phylogeny itself treated as a parameter with a prior distribution (a "tree prior"). This prior distribution is often a variant of the stochastic birth-death process, which models speciation events, extinction events, and sampling events (of extinct and/or extant lineages). However, the samples produced by this process are observations, so their probability should be viewed as a likelihood rather than a prior probability. We show that treating the samples as part of the prior results in incorrect marginal likelihood estimates and can result in model-comparison approaches disfavoring the best model within a set of candidate models. The ability to correctly compare the fit of competing tree models is critical to accurate phylogenetic estimates, especially of divergence times, and also to studying the processes that govern lineage diversification. We outline potential remedies, and provide guidance for researchers interested in comparing the fit of competing tree models.

A subterranean adaptive radiation of amphipods in Europe

Adaptive radiations are bursts of evolutionary species diversification that have contributed to much of the species diversity on Earth. An exception is modern Europe, where descendants of ancient adaptive radiations went extinct, and extant adaptive radiations are small, recent and narrowly confined. However, not all legacy of old radiations has been lost. Subterranean environments, which are dark and food-deprived, yet buffered from climate change, have preserved ancient lineages. Here we provide evidence of an entirely subterranean adaptive radiation of the amphipod genus Niphargus, counting hundreds of species. Our modelling of lineage diversification and evolution of morphological and ecological traits using a time-calibrated multilocus phylogeny suggests a major adaptive radiation, comprised of multiple subordinate adaptive radiations. Their spatio-temporal origin coincides with the uplift of carbonate massifs in South-Eastern Europe 15 million years ago. Emerging subterranean environments likely provided unoccupied, predator-free space, constituting ecological opportunity, a key trigger of adaptive radiation. This discovery sheds new light on the biodiversity of Europe.

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.