Speciation Process Research Articles

The genetic origins of species boundaries at subtropical and temperate ecoregions in the North American racers (Coluber constrictor).

Phylogeographically structured lineages are a common outcome of range-wide population genetic studies. In the southeastern United States, disconnection between populations found at the intersection of the southeastern coastal plains of peninsular Florida and the southeastern plains of the adjacent continent is readily apparent among many plants and animals. However, the timing and maintenance of species boundaries between these distinctly different subtropical and temperate regions remains unknown for all organisms studied there. Using genome-scale data, we examine the timing of origins, gene flow, and the movement of genes under selection in unique ecoregions within the North American racers (Coluber constrictor). Isolation-migration models along with tests of genome-wide selection, locus-environment associations, and spatial and genomic clines demonstrate that two unrecognized species are present and are in contact at the boundary of these two ecoregions. We show that selection at several loci associated with unique environments have maintained species boundaries despite constant levels of gene flow between these lineages over thousands of generations. This research provides a new avenue of research to examine speciation processes in poorly studied biodiversity hotspots.

Postmating prezygotic isolation occurs at two levels of divergence in Drosophila recens and D. subquinaria.

Identifying the presence and strength of reproductive isolating barriers is necessary to understand how species form and then remain distinct in the face of ongoing gene flow. Here we study reproductive isolation at two stages of the speciation process in the closely related mushroom-feeding species Drosophila recens and D. subquinaria. We assess three isolating barriers that occur after mating, including the number of eggs laid, the proportion of eggs laid that hatched, and the number of adult offspring from a single mating. First, all three reproductive barriers are present between D. recens females and D. subquinaria males, which are at the late stages of speciation but still produce fertile daughters through which gene flow can occur. There is no evidence for geographic variation in any of these traits, concurrent with patterns of behavioral isolation. Second, all three of these reproductive barriers are strong between geographically distant conspecific populations of D. subquinaria, which are in the early stages of speciation and show genetic differentiation and asymmetric behavioral discrimination. The reduction in the number of eggs laid is asymmetric, consistent with patterns in behavioral isolation, and suggests the evolution of postmating prezygotic isolation due to cascade reinforcement against mating with D. recens. In summary, not only may postmating prezygotic reproductive barriers help maintain isolation between D. recens and D. subquinaria but they may also drive the earliest stages of isolation within D. subquinaria.

Testing relationships between multiple regional features and biogeographic processes of speciation, extinction, and dispersal.

The spatial and environmental features of regions where clades are evolving are expected to impact biogeographic processes such as speciation, extinction, and dispersal. Any number of regional features (such as elevation, distance, area, etc.) may be directly or indirectly related to these processes. For example, it may be that distances or differences in elevation or both may limit dispersal rates. However, it is difficult to disentangle which features are most strongly related to rates of different processes. Here, we present an extensible Multi-feature Feature-Informed GeoSSE (MultiFIG) model that allows for the simultaneous investigation of any number of regional features. MultiFIG provides a conceptual framework for incorporating large numbers of features of different types, including categorical, quantitative, within-region, and between-region features, along with a mathematical framework for translating those features into biogeographic rates for statistical hypothesis testing. Using traditional Bayesian parameter estimation and reversible-jump Markov chain Monte Carlo, MultiFIG allows for the exploration of models with different numbers and combinations of feature-effect parameters, and generates estimates for the strengths of relationships between each regional feature and core process. We validate this model with a simulation study covering a range of scenarios with different numbers of regions, tree sizes, and feature values. We also demonstrate the application of MultiFIG with an empirical case study of the South American lizard genus Liolaemus, investigating sixteen regional features related to area, distance, and elevation. Our results show two important feature-process relationships: a negative distance/dispersal relationship, and a negative area/extinction relationship. Interestingly, although speciation rates were found to be higher in Andean versus non-Andean regions, the model did not assign significance to Andean- or elevation-related parameters. These results highlight the need to consider multiple regional features in biogeographic hypothesis testing.

Congruent and Hierarchical Intra-Lake Subdivisions from Nuclear and Mitochondrial Data of a Lake Baikal Shoreline Amphipod

A central goal of molecular studies on ancient lake faunas is to resolve the origin and phylogeny of their strikingly diverse endemic species flocks. Another equally intriguing goal is to understand the integrity of individual morphologically diagnosed species, which should help to perceive the nature and speed of the speciation process, and the true biological species diversity. In the uniquely diverse Lake Baikal amphipod crustaceans, molecular data from shallow-water species have often disclosed their cryptic subdivision into geographically segregated genetic lineages, but the evidence so far is mainly based on mitochondrial DNA. We now present a lake-wide parallel survey of both mitochondrial and multilocus nuclear genetic structuring in the common shoreline amphipod Eulimnogammarus verrucosus, known to comprise three deep, parapatric mtDNA lineages. Allele frequencies of seven nuclear allozyme loci divide the data into three main groups whose distributions exactly match the distributions of the main mitochondrial lineages S, W, and E and involve a further division of the W cluster into two subgroups. The inter-group differences involve one to four diagnostic loci and additional group-specific alleles. The transition zones are either abrupt (1 km), occur over a long segment of uninhabitable shoreline, or may be gradual with non-coincident clinal change at different loci. Mitochondrial variation is hierarchically structured, each main lineage further subdivided into 2–4 parapatric sublineages or phylogroups, and patterns of further local segregation are seen in some of them. Despite the recurring observations of cryptic diversity in Baikalian amphipods, the geographical subdivisions and clade depths do not match in different taxa, defying a common explanation for the diversification in environmental history.

A bird’s-eye view reveals no fixed differences in plumage coloration between divergent populations of Painted Buntings

AbstractIn birds, the process of speciation is closely associated with transitions in ornamentation, including coloration, plumage pattern, and song. To investigate the origins of these shifts and their connection to genetic changes, we conducted a study on one of the most highly ornamented songbirds, the Painted Bunting (Passerina ciris). The male Painted Buntings exhibits a stunning array of colors, with a red chest, blue head, green back, green coverts, and pink rump. In addition, Painted Buntings show a high level of genetic structure, with eastern and western populations that have fixed genetic differences in both nuclear and mitochondrial genes. Using non-invasive spectrophotometry techniques, we measured the coloration of six plumage patches on 88 museum specimens of male Painted Buntings in definitive plumage from across the range of the species. We predicted that there would be divergence between the genetically distinct eastern and western populations in ornamental coloration that is perceptible to a bunting but imperceptible to a human observer. However, we measured no consistent nor substantial difference in the plumage coloration of males from different populations. The observation of substantial divergence in nuclear and mitochondrial genotype with no change in ornamental coloration between populations of a brightly colored bird has important implications for the role of sexual selection in the process of speciation.

Repeated evolution on oceanic islands: comparative genomics reveals species-specific processes in birds

Understanding the interplay between genetic drift, natural selection, gene flow, and demographic history in driving phenotypic and genomic differentiation of insular populations can help us gain insight into the speciation process. Comparing patterns across different insular taxa subjected to similar selective pressures upon colonizing oceanic islands provides the opportunity to study repeated evolution and identify shared patterns in their genomic landscapes of differentiation. We selected four species of passerine birds (Common Chaffinch Fringilla coelebs/canariensis, Red-billed Chough Pyrrhocorax pyrrhocorax, House Finch Haemorhous mexicanus and Dark-eyed/island Junco Junco hyemalis/insularis) that have both mainland and insular populations. Changes in body size between island and mainland populations were consistent with the island rule. For each species, we sequenced whole genomes from mainland and insular individuals to infer their demographic history, characterize their genomic differentiation, and identify the factors shaping them. We estimated the relative (Fst) and absolute (dxy) differentiation, nucleotide diversity (π), Tajima’s D, gene density and recombination rate. We also searched for selective sweeps and chromosomal inversions along the genome. All species shared a marked reduction in effective population size (Ne) upon island colonization. We found diverse patterns of differentiated genomic regions relative to the genome average in all four species, suggesting the role of selection in island-mainland differentiation, yet the lack of congruence in the location of these regions indicates that each species evolved differently in insular environments. Our results suggest that the genomic mechanisms involved in the divergence upon island colonization—such as chromosomal inversions, and historical factors like recurrent selection—differ in each species, despite the highly conserved structure of avian genomes and the similar selective factors involved. These differences are likely influenced by factors such as genetic drift, the polygenic nature of fitness traits and the action of case-specific selective pressures.

Phylogenetic Insights into Diversification

Species diversification—the balance between speciation and extinction—is fundamental to our understanding of how species richness varies in space and time and throughout the Tree of Life. Phylogenetic approaches provide insights into species diversification by enabling support for alternative diversification scenarios to be compared and speciation and extinction rates to be estimated. Here, we review the current toolkit available for conducting such analyses. We first highlight how modeling efforts over the past decade have fostered a notable transition from overly simplistic evolutionary scenarios to a more nuanced understanding of how and why diversification rates vary through time and across lineages. Using the latitudinal diversity gradient as a case study, we then illustrate the impact that modeling choices can have on the results obtained. Finally, we review recent progress in two areas that are still lagging behind: phylogenetic insights into microbial diversification and the speciation process.

Sperm as a speciation phenotype in promiscuous songbirds.

Sperm morphology varies considerably among species. Sperm traits may contribute to speciation if they diverge fast in allopatry and cause conspecific sperm precedence upon secondary contact. However, their role in driving prezygotic isolation has been poorly investigated. Here we test the hypothesis that, early in the speciation process, female promiscuity promotes a reduction in overlap in sperm length distributions among songbird populations. We assembled a data set of 20 pairs of populations with known sperm length distributions, a published estimate of divergence time, and an index of female promiscuity derived from extrapair paternity rates or relative testis size. We found that sperm length distributions diverged more rapidly in more promiscuous species. Faster divergence between sperm length distributions was caused by the lower variance in the trait in more promiscuous species, and not by faster divergence of the mean sperm lengths. The reduced variance is presumably due to stronger stabilizing selection on sperm length mediated by sperm competition. If divergent sperm length optima in allopatry causes conspecific sperm precedence in sympatry, which remains to be shown empirically, female promiscuity may promote prezygotic isolation and rapid speciation in songbirds.

Phylogenomic and anatomical evidence for the Late Cretaceous diversification of African characiform fishes, including a new family, under the influence of the Trans-Saharan Seaway

Abstract Geological evidence supports the occurrence of an epicontinental Trans-Saharan Seaway bisecting the African continent during the Late Cretaceous to early Paleogene. The seaway formed a wide saltwater channel connecting the Neotethys with the South Atlantic, yet no previous study has investigated its impact on freshwater fish diversification. Phylogenomic data and time-calibrated trees indicate a Late Cretaceous signature for the appearance of three modern lineages of characiform fishes. Phylogenetic analyses using ultraconserved elements of 83 characiforms reveals that Alestidae, Hepsetus, and Lepidarchidae fam. nov. originated during the Santonian-Campanian of the Late Cretaceous (84–77.5 million years ago; Ma). Lepidarchidae consists of two monotypic taxa not previously recognized as sister species: the Niger tetra Arnoldichthys endemic to the lower Niger and Ogun rivers of Nigeria, and the dwarf jellybean tetra Lepidarchus from coastal rivers of Ghana, Côte d'Ivoire, Liberia, Sierra Leone, and Guinea. Microcomputed tomography scans (µCT) of 117 characiforms provide three novel morphological characters supporting Hepsetus and Lepidarchidae, four characters for monophyly of Lepidarchidae and five for a restricted Alestidae. The Santonian-Campanian divergence indicates allopatric speciation processes influenced by the Trans-Saharan Seaway, partitioning the African ichthyofauna in a west-east orientation. The timing for African characiform cladogenesis aligns with the Cenomanian fossil record and is circa 16–23 Ma younger than the earliest characiform-like fossils from Late Cretaceous outcrops of Morocco and Sudan. This study highlights the magnitude of Cretaceous transgression events shaping the freshwater biota and gaps in our understanding of the evolutionary history and paleobiogeography of ray-finned fishes across the African continent.

Common misconceptions of speciation.

Speciation is a complex process that can unfold in many different ways. Speciation researchers sometimes simplify core principles in their writing in a way that implies misconceptions about the speciation process. While we think that these misconceptions are usually inadvertently implied (and not actively believed) by the researchers, they nonetheless risk warping how external readers understand speciation. Here we highlight six misconceptions of speciation that are especially widespread. First, species are implied to be clearly and consistently defined entities in nature, whereas in reality species boundaries are often fuzzy and semipermeable. Second, speciation is often implied to be 'good', which is two-fold problematic because it implies both that evolution has a goal and that speciation universally increases the chances of lineage persistence. Third, species-poor clades with species-rich sister clades are considered 'primitive' or 'basal', falsely implying a ladder of progress. Fourth, the evolution of species is assumed to be strictly tree-like, but genomic findings show widespread hybridization more consistent with network-like evolution. Fifth, a lack of association between a trait and elevated speciation rates in macroevolutionary studies is often interpreted as evidence against its relevance in speciation-even if microevolutionary case studies show that it is relevant. Sixth, obvious trait differences between species are sometimes too readily assumed to be (i) barriers to reproduction, (ii) a stepping-stone to inevitable speciation, or (iii) reflective of the species' whole divergence history. In conclusion, we call for caution, particularly when communicating science, because miscommunication of these ideas provides fertile ground for misconceptions to spread.

That's Not a Hybrid: How to Distinguish Patterns ofAdmixture and Isolation By Distance.

Describing naturally occurring genetic variation is a fundamental goal of molecular phylogeography and population genetics. Popular methods for this task include STRUCTURE, a model-based algorithm that assigns individuals to genetic clusters, and principal component analysis (PCA), a parameter-free method. The ability of STRUCTURE to infer mixed ancestry makes it popular for documenting natural hybridisation, which is of considerable interest to evolutionary biologists, given that such systems provide a window into the speciation process. Yet, STRUCTURE can produce misleading results when its underlying assumptions are violated, like when genetic variation is distributed continuously across geographic space. To test the ability of STRUCTURE and PCA to accurately distinguish admixture from continuous variation, we use forward-time simulations to generate population genetic data under three demographic scenarios: two involving admixture and one with isolation by distance (IBD). STRUCTURE and PCA alone cannot distinguish admixture from IBD, but complementing these analyses with triangle plots, which visualise hybrid index against interclass heterozygosity, provides more accurate inference of demographic history, especially in cases of recent admixture. We demonstrate that triangle plots are robust to missing data, while STRUCTURE and PCA are not, and show that setting a low allele frequency difference threshold for ancestry-informative marker (AIM) identification can accurately characterise the relationship between hybrid index and interclass heterozygosity across demographic histories of admixture and range expansion. While STRUCTURE and PCA provide useful summaries of genetic variation, results should be paired with triangle plots before admixture is inferred.

The burst of satellite DNA in Leptidea wood white butterflies and their putative role in karyotype evolution.

Satellite DNAs (satDNAs) are abundant components of eukaryotic genomes, playing pivotal roles in chromosomal organization, genome stability, and evolution. Here, we combined cytogenetic and genomic methods to characterize the satDNAs in the genomes of Leptidea butterflies. Leptidea is characterized by the presence of a high heterochromatin content, large genomes, and extensive chromosomal reshuffling as well as the occurrence of cryptic species. We show that, in contrast to other Lepidoptera, satDNAs constitute a considerable proportion of Leptidea genomes, ranging between 4.11% and 11.05%. This amplification of satDNAs, together with the hyperactivity of transposable elements, contributes to the substantial genome expansion in Leptidea. Using chromosomal mapping, we show that, particularly LepSat01-100 and LepSat03-167 satDNAs, are preferentially localized in heterochromatin exhibiting variable distribution that may have contributed to the highly diverse karyotypes within the genus. The satDNAs also exhibit W-chromosome accumulation, suggesting their involvement in sex chromosome evolution. Our results provide insights into the dynamics of satDNAs in Lepidoptera genomes and highlight their role in genome expansion and chromosomal organization, which could influence the speciation process. The high proportion of repetitive DNAs in the genomes of Leptidea underscores the complex evolutionary dynamics revealing the interplay between repetitive DNAs and genomic architecture in the genus.

Ecological speciation in East African freshwater crabs of the genus Arcopotamonautes Bott, 1955 across a lake-river boundary in the Lake Malawi catchment (Potamoidea: Potamonautidae: Potamonatinae)

Abstract Geological, climate and ecosystem changes in Africa likely influenced speciation of Afrotropical freshwater crabs. In total, the subfamily Potamonautinae comprises over 120 species, and this diversity provides a valuable opportunity to explore speciation processes. Here we study diversification of potamonautid crabs in the Lake Malawi catchment, and investigate whether speciation has taken place across a lake-river boundary. Specifically, we reconstruct evolutionary relationships of the Malawi blue crab, Arcopotamonautes orbitospinus (Cunnington, 1907), an endemic of Lake Malawi, and of A. montivagus (Chace, 1953) from rivers and streams draining into Lake Malawi, and smaller lakes within this catchment. Our phylogenetic analysis of over 28,000 single nucleotide polymorphisms shows a monophyletic A. orbitospinus nested within a clade otherwise comprised of A. montivagus from across the Lake Malawi catchment (A. montivagus Group I). We also identified a second allopatric clade of A. montivagus from the Rungwe mountains of Tanzania, and neighbouring Zambia (A. montivagus Group II). Morphological differences were apparent between all three groups. Collectively these results show A. montivagus is a paraphyletic riverine taxon that has diversified in allopatry, and that this species entered Lake Malawi and seeded the specialised heavily armoured lacustrine species, A. orbitospinus. We hypothesise that formation of deep-water conditions within Lake Malawi, together with differences in predation pressures between the rivers and lake, provided ecological opportunities for natural selection to drive speciation across the lake-river boundary. We conclude that geographical separation and ecological adaptation are potentially important drivers of evolutionary diversification in these enigmatic freshwater crabs.

Inheritance of signs of parent species by hybrids of Russet, Yellow and Speckled ground squirrels (<i>Spermophilus</i>, Sciuridae, Rodentia)

The inheritance of size, color and bioacoustic characteristics of Russet (Spermophilus major), Yellow (S. fulvus) and Speckled (S. suslicus) ground squirrels in hybrids differing in their genetic status were studied. In a hybrid population of Russet and Yellow ground squirrels, 10 individuals of S. major, 10 individuals of S. fulvus and 40 hybrids of S. major × S. fulvus were analyzed; in a hybrid population of Russet and Speckled ground squirrels, 11 individuals of S. major, 11 individuals of S. suslicus and 24 hybrids of S. major × S. suslicus were analyzed. Hybrid individuals different in genetic status have been shown to demonstrate differentiation in the vector space of the variability range of the parental species. At the same time, both a shift in some categories of hybrids towards one of the hybridizing species and a significant deviation are noted. The results obtained indicate an increase in the level of variability in size, color and bioacoustic characters in hybrid populations, associated with the erosion of the divergent hiatus of specific features of the parental forms due to the formation of a differentiated hybrid population. As hybrid individuals with different combinations of parental traits accumulate in the population, the situation arises when a sufficient number of hybrids with an overall combination of parental traits (Hcomb) appear in the hybridogenic population. In the hybrid population of the Russet and Yellow ground squirrels, the proportion of such hybrids, according to our data, is 22.5% (n = 40), and in the hybrid population of the Russet and Speckled ground squirrels it is 12.5% (n = 24). This category of hybrid individuals can be considered as possible material for further microevolutionary events and the process of speciation.

Taxonomic revision and evolutionary history of the climbing mice in eastern Africa (Dendromus mystacalis clade): the role of elevation and geographical barriers in the speciation process

Taxonomic revision and evolutionary history of the climbing mice in eastern Africa (Dendromus mystacalis clade): the role of elevation and geographical barriers in the speciation process

Speciation and evolution of growth form in Adesmia D. C. (Dalbergieae, Fabaceae): the relevance of Andean uplift and aridification.

The Andean uplift and the concomitant aridification drove the rapid diversification of several plant lineages that were able to colonize warmer and drier habitats at low elevations and wetter and colder habitats at high elevations. These transitions may be facilitated by shifts in plant strategies to cope with drought and cold, which in turn can trigger episodes of accelerated species diversification. Here, we used four nuclear DNA markers to infer phylogenetic relationships of 80 Adesmia species of annuals, perennial herbs, shrubs and small shrubs that occur in Chile and Argentina. We reconstructed ancestral states for area, climatic niche and growth form to explore how Andean uplift and aridification promoted Adesmia diversification. We also performed logistic and linear regression analyses between different components of growth form (life span, woodiness and plant height) and climate. Finally, we estimated speciation rates across the phylogeny. Our results suggest that the ancestor of Chilean Adesmia was a perennial herb that probably originated in the high Andes of northern and central Chile. The low elevations of Central Chile were colonized in the late Miocene, whereas the high latitudes of Patagonia and the hyperarid coastal Atacama Desert were colonized repeatedly since Pliocene by lineages with different growth forms. Multiple and bidirectional transitions between annual and perennial habits and between herbaceous and woody habits were detected. These shifts were not correlated with climate, suggesting that the different growth forms are alternative and successful strategies to survive unfavorable seasons of both desert and high Andes. Net diversification analysis indicated a constant rate of diversification, suggesting that the high species diversity of Adesmia that occur in Chile is due to a uniform speciation process rather than to accelerated episodes of speciation.

Understanding species limits through the formation of phylogeographic lineages.

The outcomes of speciation across organismal dimensions (e.g., ecological, genetic, phenotypic) are often assessed using phylogeographic methods. At one extreme, reproductively isolated lineages represent easily delimitable species differing in many or all dimensions, and at the other, geographically distinct genetic segments introgress across broad environmental gradients with limited phenotypic disparity. In the ambiguous gray zone of speciation, where lineages are genetically delimitable but still interacting ecologically, it is expected that these lineages represent species in the context of ontology and the evolutionary species concept when they are maintained over time with geographically well-defined hybrid zones, particularly at the intersection of distinct environments. As a result, genetic structure is correlated with environmental differences and not space alone, and a subset of genes fail to introgress across these zones as underlying genomic differences accumulate. We present a set of tests that synthesize species delimitation with the speciation process. We can thereby assess historical demographics and diversification processes while understanding how lineages are maintained through space and time by exploring spatial and genome clines, genotype-environment interactions, and genome scans for selected loci. Employing these tests in eight lineage-pairs of snakes in North America, we show that six pairs represent 12 "good" species and that two pairs represent local adaptation and regional population structure. The distinct species pairs all have the signature of divergence before or near the mid-Pleistocene, often with low migration, stable hybrid zones of varying size, and a subset of loci showing selection on alleles at the hybrid zone corresponding to transitions between distinct ecoregions. Locally adapted populations are younger, exhibit higher migration, and less ecological differentiation. Our results demonstrate that interacting lineages can be delimited using phylogeographic and population genetic methods that properly integrate spatial, temporal, and environmental data.

Secondary contact zone and genetic introgression in closely related haplodiploid social spider mites.

How frequently hybridisation and gene flow occur in the contact zones of diverging taxa is important for understanding the speciation process. Stigmaeopsis sabelisi and Stigmaeopsis miscanthi high-aggression form (hereafter, S. miscanthi HG) are haplodiploid, social spider mites that infest the Chinese silver grass, Miscanthus sinensis. These two species are closely related and parapatrically distributed in Japan. In mountainous areas, S. sabelisi and S. miscanthi HG are often found in the highlands and lowlands, respectively, suggesting that they are in contact at intermediate altitudes. It is estimated that they diverged from their common ancestors distributed in subtropical regions (south of Japan) during the last glacial period, expanded their distribution into the Japanese Archipelago, and came to have such a parapatric distribution (secondary contact). As their reproductive isolation is strong but incomplete, hybridisation and genetic introgression are expected at their distributional boundaries. In this study, we investigated their spatial distribution patterns along the elevation on Mt. Amagi using male morphological differences, and investigated their hybridisation status using single-nucleotide polymorphisms by MIG-seq. We found their contact zone at altitudes of 150-430 m, suggesting that their contact zone is prevalent in the parapatric area, which is in line with a previous study. Interspecific mating was predicted based on the sex ratio in the contact zone. No obvious hybrids were found, but genetic introgression was detected although it was extremely low.

Bursts of Rapid Diversification, Dispersals Out of Southern Africa, and Two Origins of Dioecy Punctuate the Evolution of Asparagus.

The genus Asparagus arose ∼9 to 15 million years ago (Ma), and transitions from hermaphroditism to dioecy (separate sexes) occurred ∼3 to 4 Ma. Roughly 27% of extant Asparagus species are dioecious, while the remaining are bisexual with monoclinous flowers. As such, Asparagus is an ideal model taxon for studying the early stages of dioecy and sex chromosome evolution in plants. Until now, however, understanding of diversification and shifts from hermaphroditism to dioecy in Asparagus has been hampered by the lack of robust species tree estimates for the genus. In this study, a genus-wide phylogenomic analysis including 1,726 nuclear loci and comprehensive species sampling supports two independent origins of dioecy in Asparagus-first in a widely distributed Eurasian clade and then in a clade restricted to the Mediterranean Basin. Modeling of ancestral biogeography indicates that both dioecy origins were associated with range expansion out of southern Africa. Our findings also reveal several bursts of diversification across the phylogeny, including an initial radiation in southern Africa that gave rise to 12 major clades in the genus, and more recent radiations that have resulted in paraphyly and polyphyly among closely related species, as expected given active speciation processes. Lastly, we report that the geographic origin of domesticated garden asparagus (Asparagus officinalis L.) was likely in western Asia near the Mediterranean Sea. The presented phylogenomic framework for Asparagus is foundational for ongoing genomic investigations of diversification and functional trait evolution in the genus and contributes to its utility for understanding the origin and early evolution of dioecy and sex chromosomes.

Untangling the colonization history of the Australo-Pacific reed warblers, one of the world's great island radiations.

Island radiations, such as those of the Australo-Pacific, offer unique insight into diversification, extinction, and early speciation processes. Yet, their speciation and colonization histories are often obscured by conflicting genomic signals from incomplete lineage sorting or hybridization. Here, we integrated mitogenomes and genome-wide SNPs to unravel the evolutionary history of one of the world's most geographically widespread island radiations. The Australo-Pacific reed warblers (Acrocephalus luscinius complex) are a speciose lineage including five species that have become extinct since the 19th century and ten additional species of conservation concern. The radiation spans over 10,000 km across Australo-Papua, Micronesia and Polynesia, including the Mariana, Hawaii and Pitcairn Island archipelagos. Earlier mtDNA studies suggested a stepping-stone colonization process, resulting in archipelago-level secondary sympatry of divergent mtDNA lineages in the Mariana Islands and Marquesas. These studies hypothesised that morphologically similar species on neighbouring islands arose from ecological convergence. Using hDNA from historical museum specimens and modern genetic samples, we show that incomplete lineage sorting and/or gene flow have shaped the radiation of Australo-Pacific reed warblers rather than secondary sympatry. The nuclear genome reconstructs a simpler biogeographic history than mtDNA, showing close relationships between species in the Mariana Islands and Marquesas despite their paraphyletic mtDNA lineages. Gene flow likely involved early and late colonizing waves of the radiation before the loss of ancestral dispersive ability. Our results highlight how collection genomics can elucidate evolutionary history and inform conservation efforts for threatened species.