Incomplete lineage sorting and phenotypic evolution in marsupials.

Incomplete lineage sorting (ILS) makes ancestral genetic polymorphisms persist during rapid speciation events, inducing incongruences between gene trees and species trees. ILS has complicated phylogenetic inference in many lineages, including hominids. However, we lack empirical evidence that ILS leads to incongruent phenotypic variation. Here, we performed phylogenomic analyses to show that the South American monito del monte is the sister lineage of all Australian marsupials, although over 31% of its genome is closer to the Diprotodontia than to other Australian groups due to ILS during ancient radiation. Pervasive conflicting phylogenetic signals across the whole genome are consistent with some of the morphological variation among extant marsupials. We detected hundreds of genes that experienced stochastic fixation during ILS, encoding the same amino acids in non-sister species. Using functional experiments, we confirm how ILS may have directly contributed to hemiplasy in morphological traits that were established during rapid marsupial speciation ca. 60 mya.

Mucosal fungi promote gut barrier function and social behavior via Type 17 immunity.

Fungal communities (the mycobiota) are an integral part of the gut microbiota, and the disruption of their integrity contributes to local and gut-distal pathologies. Yet, the mechanisms by which intestinal fungi promote homeostasis remain unclear. We characterized the mycobiota biogeography along the gastrointestinal tract and identified a subset of fungi associated with the intestinal mucosa of mice and humans. Mucosa-associated fungi (MAF) reinforced intestinal epithelial function and protected mice against intestinal injury and bacterial infection. Notably, intestinal colonization with a defined consortium of MAF promoted social behavior in mice. The gut-local effects on barrier function were dependent on IL-22 production by CD4+ T helper cells, whereas the effects on social behavior were mediated through IL-17R-dependent signaling in neurons. Thus, the spatial organization of the gut mycobiota is associated with host-protective immunity and epithelial barrier function and might be a driver of the neuroimmune modulation of mouse behavior through complementary Type 17 immune mechanisms.

Charting the Complexity of the Marine Microbiome through Single-Cell Genomics.

Marine bacteria and archaea play key roles in global biogeochemistry. To improve our understanding of this complex microbiome, we employed single-cell genomics and a randomized, hypothesis-agnostic cell selection strategy to recover 12,715 partial genomes from the tropical and subtropical euphotic ocean. A substantial fraction of known prokaryoplankton coding potential was recovered from a single, 0.4 mL ocean sample, which indicates that genomic information disperses effectively across the globe. Yet, we found each genome to be unique, implying limited clonality within prokaryoplankton populations. Light harvesting and secondary metabolite biosynthetic pathways were numerous across lineages, highlighting the value of single-cell genomics to advance the identification of ecological roles and biotechnology potential of uncultured microbial groups. This genome collection enabled functional annotation and genus-level taxonomic assignments for >80% of individual metagenome reads from the tropical and subtropical surface ocean, thus offering a model to improve reference genome databases for complex microbiomes.

Microbiota Diurnal Rhythmicity Programs Host Transcriptome Oscillations.

The intestinal microbiota undergoes diurnal compositional and functional oscillations that affect metabolic homeostasis, but the mechanisms by which the rhythmic microbiota influences host circadian activity remain elusive. Using integrated multi-omics and imaging approaches, we demonstrate that the gut microbiota features oscillating biogeographical localization and metabolome patterns that determine the rhythmic exposure of the intestinal epithelium to different bacterial species and their metabolites over the course of a day. This diurnal microbial behavior drives, in turn, the global programming of the host circadian transcriptional, epigenetic, and metabolite oscillations. Surprisingly, disruption of homeostatic microbiome rhythmicity not only abrogates normal chromatin and transcriptional oscillations of the host, but also incites genome-wide de novo oscillations in both intestine and liver, thereby impacting diurnal fluctuations of host physiology and disease susceptibility. As such, the rhythmic biogeography and metabolome of the intestinal microbiota regulates the temporal organization and functional outcome of host transcriptional and epigenetic programs.

The dawn of the tropical Atlantic invasion into the Mediterranean Sea.

The Mediterranean Sea is a marine biodiversity hotspot already affected by climate-driven biodiversity collapses. Its highly endemic fauna is at further risk if global warming triggers an invasion of tropical Atlantic species. Here, we combine modern species occurrences with a unique paleorecord from the Last Interglacial (135 to 116 ka), a conservative analog of future climate, to model the future distribution of an exemplary subset of tropical West African mollusks, currently separated from the Mediterranean by cold upwelling off north-west Africa. We show that, already under an intermediate climate scenario (RCP 4.5) by 2050, climatic connectivity along north-west Africa may allow tropical species to colonize a by then largely environmentally suitable Mediterranean. The worst-case scenario RCP 8.5 leads to a fully tropicalized Mediterranean by 2100. The tropical Atlantic invasion will add to the ongoing Indo-Pacific invasion through the Suez Canal, irreversibly transforming the entire Mediterranean into a novel ecosystem unprecedented in human history.

Chromosomal evolution, environmental heterogeneity, and migration drive spatial patterns of species richness in Calochortus (Liliaceae).

We used nuclear genomic data and statistical models to evaluate the ecological and evolutionary processes shaping spatial variation in species richness in Calochortus (Liliaceae, 74 spp.). Calochortus occupies diverse habitats in the western United States and Mexico and has a center of diversity in the California Floristic Province, marked by multiple orogenies, winter rainfall, and highly divergent climates and substrates (including serpentine). We used sequences of 294 low-copy nuclear loci to produce a time-calibrated phylogeny, estimate historical biogeography, and test hypotheses regarding drivers of present-day spatial patterns in species number. Speciation and species coexistence require reproductive isolation and ecological divergence, so we examined the roles of chromosome number, environmental heterogeneity, and migration in shaping local species richness. Six major clades-inhabiting different geographic/climatic areas, and often marked by different base chromosome numbers (n = 6 to 10)-began diverging from each other ~10.3 Mya. As predicted, local species number increased significantly with local heterogeneity in chromosome number, elevation, soil characteristics, and serpentine presence. Species richness is greatest in the Transverse/Peninsular Ranges where clades with different chromosome numbers overlap, topographic complexity provides diverse conditions over short distances, and several physiographic provinces meet allowing immigration by several clades. Recently diverged sister-species pairs generally have peri-patric distributions, and maximum geographic overlap between species increases over the first million years since divergence, suggesting that chromosomal evolution, genetic divergence leading to gametic isolation or hybrid inviability/sterility, and/or ecological divergence over small spatial scales may permit species co-occurrence.

Saccharomycotina yeasts defy long-standing macroecological patterns.

The Saccharomycotina yeasts ("yeasts" hereafter) are a fungal clade of scientific, economic, and medical significance. Yeasts are highly ecologically diverse, found across a broad range of environments in every biome and continent on earth; however, little is known about what rules govern the macroecology of yeast species and their range limits in the wild. Here, we trained machine learning models on 12,816 terrestrial occurrence records and 96 environmental variables to infer global distribution maps at ~1 km2 resolution for 186 yeast species (~15% of described species from 75% of orders) and to test environmental drivers of yeast biogeography and macroecology. We found that predicted yeast diversity hotspots occur in mixed montane forests in temperate climates. Diversity in vegetation type and topography were some of the greatest predictors of yeast species richness, suggesting that microhabitats and environmental clines are key to yeast diversity. We further found that range limits in yeasts are significantly influenced by carbon niche breadth and range overlap with other yeast species, with carbon specialists and species in high-diversity environments exhibiting reduced geographic ranges. Finally, yeasts contravene many long-standing macroecological principles, including the latitudinal diversity gradient, temperature-dependent species richness, and a positive relationship between latitude and range size (Rapoport's rule). These results unveil how the environment governs the global diversity and distribution of species in the yeast subphylum. These high-resolution models of yeast species distributions will facilitate the prediction of economically relevant and emerging pathogenic species under current and future climate scenarios.

Evolutionary norm-breaking and extinction in the marine tropics.

Evolutionary innovations, defined as character states that transcend clade norms, are often studied in an exclusively phylogenetic context, but their distribution in time and space indicates that geography also influences the evolution of new ecological, morphological, and physiological traits. In an analysis of 99 fossillzable, norm-breaking innovations in tropical marine Neogene molluscan clades that arose uniquely in either (but not in both) the Indo-West Pacific (IWP) or Atlantic-East Pacific (AEP) realms, I show that there are far more innovations in the IWP (79%) than those in the AEP (21%). Most of the innovations are interpretable as defensive or competitive adaptations or as indicators of extreme habitat specialization. Although the innovations arose in taxonomically rich biotas, only 9% are associated with subclades comprising 10 or more species each, indicating that they contributed little to overall taxonomic richness. Compilations of extant species in 30 pantropical molluscan clades show that the IWP accounts for 71% of tropical shallow-water species, implying that the per-species incidence of norm-breaking innovations is higher there than in the AEP. Only 5% of innovations became extinct in the IWP as compared with 38% in the AEP, mirroring a similar difference in the magnitudes of Late Miocene and later taxonomic extinction in the two realms. These data imply that large-scale disruption strongly limits norm-breaking innovation. Opportunities for adaptive innovation are therefore likely to be few in today's heavily overexploited and disturbed biosphere.

Plants maintain climate fidelity in the face of dynamic climate change.

Plants will experience considerable changes in climate within their geographic ranges over the next several decades. They may respond by exhibiting niche flexibility and adapting to changing climates. Alternatively, plant taxa may exhibit climate fidelity, shifting their geographic distributions to track their preferred climates. Here, we examine the responses of plant taxa to changing climates over the past 18,000 y to evaluate the extent to which the 16 dominant plant taxa of North America have exhibited climate fidelity. We find that 75% of plant taxa consistently exhibit climate fidelity over the past 18,000 y, even during the times of most extreme climate change. Of the four taxa that do not consistently exhibit climate fidelity, three-elm (Ulmus), beech (Fagus), and ash (Fraxinus)-experience a long-term shift in their realized climatic niche between the early Holocene and present day. Plant taxa that migrate longer distances better maintain consistent climatic niches across transition periods during times of the most extreme climate change. Today, plant communities with the highest climate fidelity are found in regions with high topographic and microclimate heterogeneity that are expected to exhibit high climate resilience, allowing plants to shift distributions locally and adjust to some amount of climate change. However, once the climate change buffering of the region is exceeded, these plant communities will need to track climates across broader landscapes but be challenged to do so because of the low habitat connectivity of the regions.

Speciation across the Earth driven by global cooling in terrestrial orchids.

Although climate change has been implicated as a major catalyst of diversification, its effects are thought to be inconsistent and much less pervasive than localized climate or the accumulation of species with time. Focused analyses of highly speciose clades are needed in order to disentangle the consequences of climate change, geography, and time. Here, we show that global cooling shapes the biodiversity of terrestrial orchids. Using a phylogeny of 1,475 species of Orchidoideae, the largest terrestrial orchid subfamily, we find that speciation rate is dependent on historic global cooling, not time, tropical distributions, elevation, variation in chromosome number, or other types of historic climate change. Relative to the gradual accumulation of species with time, models specifying speciation driven by historic global cooling are over 700 times more likely. Evidence ratios estimated for 212 other plant and animal groups reveal that terrestrial orchids represent one of the best-supported cases of temperature-spurred speciation yet reported. Employing >2.5 million georeferenced records, we find that global cooling drove contemporaneous diversification in each of the seven major orchid bioregions of the Earth. With current emphasis on understanding and predicting the immediate impacts of global warming, our study provides a clear case study of the long-term impacts of global climate change on biodiversity.

The build-up of the present-day tropical diversity of tetrapods.

The extraordinary number of species in the tropics when compared to the extra-tropics is probably the most prominent and consistent pattern in biogeography, suggesting that overarching processes regulate this diversity gradient. A major challenge to characterizing which processes are at play relies on quantifying how the frequency and determinants of tropical and extra-tropical speciation, extinction, and dispersal events shaped evolutionary radiations. We address this question by developing and applying spatiotemporal phylogenetic and paleontological models of diversification for tetrapod species incorporating paleoenvironmental variation. Our phylogenetic model results show that area, energy, or species richness did not uniformly affect speciation rates across tetrapods and dispute expectations of a latitudinal gradient in speciation rates. Instead, both neontological and fossil evidence coincide in underscoring the role of extra-tropical extinctions and the outflow of tropical species in shaping biodiversity. These diversification dynamics accurately predict present-day levels of species richness across latitudes and uncover temporal idiosyncrasies but spatial generality across the major tetrapod radiations.

Changes in parrot diversity after human arrival to the Caribbean.

Humans did not arrive on most of the world's islands until relatively recently, making islands favorable places for disentangling the timing and magnitude of natural and anthropogenic impacts on species diversity and distributions. Here, we focus on Amazona parrots in the Caribbean, which have close relationships with humans (e.g., as pets as well as sources of meat and colorful feathers). Caribbean parrots also have substantial fossil and archaeological records that span the Holocene. We leverage this exemplary record to showcase how combining ancient and modern DNA, along with radiometric dating, can shed light on diversification and extinction dynamics and answer long-standing questions about the magnitude of human impacts in the region. Our results reveal a striking loss of parrot diversity, much of which took place during human occupation of the islands. The most widespread species, the Cuban Parrot, exhibits interisland divergences throughout the Pleistocene. Within this radiation, we identified an extinct, genetically distinct lineage that survived on the Turks and Caicos until Indigenous human settlement of the islands. We also found that the narrowly distributed Hispaniolan Parrot had a natural range that once included The Bahamas; it thus became "endemic" to Hispaniola during the late Holocene. The Hispaniolan Parrot also likely was introduced by Indigenous people to Grand Turk and Montserrat, two islands where it is now also extirpated. Our research demonstrates that genetic information spanning paleontological, archaeological, and modern contexts is essential to understand the role of humans in altering the diversity and distribution of biota.

Landscape dynamics and diversification of the megadiverse South American freshwater fish fauna.

Landscape dynamics are widely thought to govern the tempo and mode of continental radiations, yet the effects of river network rearrangements on dispersal and lineage diversification remain poorly understood. We integrated an unprecedented occurrence dataset of 4,967 species with a newly compiled, time-calibrated phylogeny of South American freshwater fishes-the most species-rich continental vertebrate fauna on Earth-to track the evolutionary processes associated with hydrogeographic events over 100 Ma. Net lineage diversification was heterogeneous through time, across space, and among clades. Five abrupt shifts in net diversification rates occurred during the Paleogene and Miocene (between 30 and 7 Ma) in association with major landscape evolution events. Net diversification accelerated from the Miocene to the Recent (c. 20 to 0 Ma), with Western Amazonia having the highest rates of in situ diversification, which led to it being an 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 the Early Miocene (c. 23 to 16 Ma) uplift of the Serra do Mar and Serra da Mantiqueira and the Late Miocene (c. 10 Ma) uplift of the Northern Andes and associated formation of the modern transcontinental Amazon River. The combination of high diversification rates and extensive biotic interchange associated with Western Amazonia yielded its extraordinary contemporary richness and phylogenetic endemism. Our results support the hypothesis that landscape dynamics, which shaped the history of drainage basin connections, strongly affected the assembly and diversification of basin-wide fish faunas.

Capturing patterns of evolutionary relatedness with reflectance spectra to model and monitor biodiversity.

Biogeographic history can set initial conditions for vegetation community assemblages that determine their climate responses at broad extents that land surface models attempt to forecast. Numerous studies have indicated that evolutionarily conserved biochemical, structural, and other functional attributes of plant species are captured in visible-to-short wavelength infrared, 400 to 2,500 nm, reflectance properties of vegetation. Here, we present a remotely sensed phylogenetic clustering and an evolutionary framework to accommodate spectra, distributions, and traits. Spectral properties evolutionarily conserved in plants provide the opportunity to spatially aggregate species into lineages (interpreted as "lineage functional types" or LFT) with improved classification accuracy. In this study, we use Airborne Visible/Infrared Imaging Spectrometer data from the 2013 Hyperspectral Infrared Imager campaign over the southern Sierra Nevada, California flight box, to investigate the potential for incorporating evolutionary thinking into landcover classification. We link the airborne hyperspectral data with vegetation plot data from 1372 surveys and a phylogeny representing 1,572 species. Despite temporal and spatial differences in our training data, we classified plant lineages with moderate reliability (Kappa = 0.76) and overall classification accuracy of 80.9%. We present an assessment of classification error and detail study limitations to facilitate future LFT development. This work demonstrates that lineage-based methods may be a promising way to leverage the new-generation high-resolution and high return-interval hyperspectral data planned for the forthcoming satellite missions with sparsely sampled existing ground-based ecological data.

Model misspecification misleads inference of the spatial dynamics of disease outbreaks.

Epidemiology has been transformed by the advent of Bayesian phylodynamic models that allow researchers to infer the geographic history of pathogen dispersal over a set of discrete geographic areas [1, 2]. These models provide powerful tools for understanding the spatial dynamics of disease outbreaks, but contain many parameters that are inferred from minimal geographic information (i.e., the single area in which each pathogen was sampled). Consequently, inferences under these models are inherently sensitive to our prior assumptions about the model parameters. Here, we demonstrate that the default priors used in empirical phylodynamic studies make strong and biologically unrealistic assumptions about the underlying geographic process. We provide empirical evidence that these unrealistic priors strongly (and adversely) impact commonly reported aspects of epidemiological studies, including: 1) the relative rates of dispersal between areas; 2) the importance of dispersal routes for the spread of pathogens among areas; 3) the number of dispersal events between areas, and; 4) the ancestral area in which a given outbreak originated. We offer strategies to avoid these problems, and develop tools to help researchers specify more biologically reasonable prior models that will realize the full potential of phylodynamic methods to elucidate pathogen biology and, ultimately, inform surveillance and monitoring policies to mitigate the impacts of disease outbreaks.

Integrating biogeography and behavioral ecology to rapidly address biodiversity loss.

Addressing climate change and biodiversity loss will be the defining ecological, political, and humanitarian challenge of our time. Alarmingly, policymakers face a narrowing window of opportunity to prevent the worst impacts, necessitating complex decisions about which land to set aside for biodiversity preservation. Yet, our ability to make these decisions is hindered by our limited capacity to predict how species will respond to synergistic drivers of extinction risk. We argue that a rapid integration of biogeography and behavioral ecology can meet these challenges because of the distinct, yet complementary levels of biological organization they address, scaling from individuals to populations, and from species and communities to continental biotas. This union of disciplines will advance efforts to predict biodiversity's responses to climate change and habitat loss through a deeper understanding of how biotic interactions and other behaviors modulate extinction risk, and how responses of individuals and populations impact the communities in which they are embedded. Fostering a rapid mobilization of expertise across behavioral ecology and biogeography is a critical step toward slowing biodiversity loss.

Reticulate evolution of the tertiary relict Osmanthus.

When interspecific gene flow is common, species relationships are more accurately represented by a phylogenetic network than by a bifurcating tree. This study aimed to uncover the role of introgression in the evolution of Osmanthus, the only genus of the subtribe Oleinae (Oleaceae) with its distribution center in East Asia. We built species trees, detected introgression, and constructed networks using multiple kinds of sequencing data (whole genome resequencing, transcriptome sequencing, and Sanger sequencing of nrDNA) combined with concatenation and coalescence approaches. Then, based on well-understood species relationships, historical biogeographic analyses and diversification rate estimates were employed to reveal the history of Osmanthus. Osmanthus originated in mid-Miocene Europe and dispersed to the eastern Tibetan Plateau in the late Miocene. Thereafter, it continued to spread eastwards. Phylogenetic conflict is common within the 'Core Osmanthus' clade and is seen at both early and late stages of diversification, leading to hypotheses of net-like species relationships. Incomplete lineage sorting proved ineffective in explaining phylogenetic conflicts and thus supported introgression as the main cause of conflicts. This study elucidates the diversification history of a relict genus in the subtropical regions of eastern Asia and reveals that introgression had profound effects on its evolutionary history.

Biogeographic Perspectives on Human Genetic Diversification.

Modern humans originated in Africa 300,000 yr ago, and before leaving their continent of origin, they underwent a process of intense diversification involving complex demographic dynamics. Upon exiting Africa, different populations emerged on the four other inhabited continents, shaped by the interplay of various evolutionary processes, such as migrations, founder effects, and natural selection. Within each region, continental populations, in turn, diversified and evolved almost independently for millennia. As a backdrop to this diversification, introgressions from archaic species contributed to establishing different patterns of genetic diversity in different geographic regions, reshaping our understanding of our species' variability. With the increasing availability of genomic data, it has become possible to delineate the subcontinental human population structure precisely. However, the bias toward the genomic research focused on populations from the global North has limited our understanding of the real diversity of our species and the processes and events that guided different human groups throughout their evolutionary history. This perspective is part of a series of articles celebrating 40 yr since our journal, Molecular Biology and Evolution, was founded (Russo et al. 2024). The perspective is accompanied by virtual issues, a selection of papers on human diversification published by Genome Biology and Evolution and Molecular Biology and Evolution.

Integrating genomics and biogeography to unravel the origin of a mountain biota: The case of a reptile endemicity hotspot in Arabia.

Advances in genomics have greatly enhanced our understanding of mountain biodiversity, providing new insights into the complex and dynamic mechanisms that drive the formation of mountain biotas. These span from broad biogeographic patterns to population dynamics and adaptations to these environments. However, significant challenges remain in integrating large-scale and fine-scale findings to develop a comprehensive understanding of mountain biodiversity. One significant challenge is the lack of genomic data, particularly in historically understudied arid regions where reptiles are a particularly diverse vertebrate group. In the present study, we assembled a de novo genome-wide SNP dataset for the complete endemic reptile fauna of a mountain range (19 described species with more than 600 specimens sequenced), and integrated state-of-the-art biogeographic analyses at the population, species, and community level. Thus, we provide a holistic integration of how a whole endemic reptile community has originated, diversified and dispersed through a mountain system. Our results show that reptiles independently colonized the Hajar Mountains of southeastern Arabia 11 times. After colonization, species delimitation methods suggest high levels of within-mountain diversification, supporting up to 49 deep lineages. This diversity is strongly structured following local topography, with the highest peaks acting as a broad barrier to gene flow among the entire community. Interestingly, orogenic events do not seem key drivers of the biogeographic history of reptiles in this system. Instead, past climatic events seem to have had a major role in this community assemblage. We observe an increase of vicariant events from Late Pliocene onwards, coinciding with an unstable climatic period of rapid shifts between hyper-arid and semiarid conditions that led to the ongoing desertification of Arabia. We conclude that paleoclimate, and particularly extreme aridification, acted as a main driver of diversification in arid mountain systems which is tangled with the generation of highly adapted endemicity. Overall, our study does not only provide a valuable contribution to understanding the evolution of mountain biodiversity, but also offers a flexible and scalable approach that can be reproduced into any taxonomic group and at any discrete environment.

Tropical Origin, Global Diversification and Dispersal in the Pond Damselflies (Coenagrionoidea) Revealed by a New Molecular Phylogeny.

The processes responsible for the formation of Earth's most conspicuous diversity pattern, the latitudinal diversity gradient (LDG), remain unexplored for many clades in the Tree of Life. Here, we present a densely-sampled and dated molecular phylogeny for the most speciose clade of damselflies worldwide (Odonata: Coenagrionoidea), and investigate the role of time, macroevolutionary processes and biome-shift dynamics in shaping the LDG in this ancient insect superfamily. We used process-based biogeographic models to jointly infer ancestral ranges and speciation times, and to characterise within-biome dispersal and biome-shift dynamics across the cosmopolitan distribution of Coenagrionoidea. We also investigated temporal and biome-dependent variation in diversification rates. Our results uncover a tropical origin of pond damselflies and featherlegs ~ 105 Ma, while highlighting uncertainty of ancestral ranges within the tropics in deep time. Even though diversification rates have declined since the origin of this clade, global climate change and biome-shifts have slowly increased diversity in warm- and cold-temperate areas, where lineage turnover rates have been relatively higher. This study underscores the importance of biogeographic origin and time to diversify as important drivers of the LDG in pond damselflies and their relatives, while diversification dynamics have instead resulted in the formation of ephemeral species in temperate regions. Biome-shifts, although limited by tropical niche conservatism, have been the main factor reducing the steepness of the LDG in the last 30 Myr. With ongoing climate change and increasing northward range expansions of many damselfly taxa, the LDG may become less pronounced. Our results support recent calls to unify biogeographic and macroevolutionary approaches to increase our understanding of how latitudinal diversity gradients are formed and why they vary across time and among taxa.