Sister Species Pairs Research Articles

Recurrent selection shapes the genomic landscape of differentiation between a pair of host-specialized haplodiploids that diverged with gene flow.

Understanding the genetics of adaptation and speciation is critical for a complete picture of how biodiversity is generated and maintained. Heterogeneous genomic differentiation between diverging taxa is commonly documented, with genomic regions of high differentiation interpreted as resulting from differential gene flow, linked selection and reduced recombination rates. Disentangling the roles of each of these non-exclusive processes in shaping genome-wide patterns of divergence is challenging but will enhance our knowledge of the repeatability of genomic landscapes across taxa. Here, we combine whole-genome resequencing and genome feature data to investigate the processes shaping the genomic landscape of differentiation for a sister-species pair of haplodiploid pine sawflies, Neodiprion lecontei and Neodiprion pinetum. We find genome-wide correlations between genome features and summary statistics are consistent with pervasive linked selection, with patterns of diversity and divergence more consistently predicted by exon density and recombination rate than the neutral mutation rate (approximated by dS). We also find that both global and local patterns of FST, dXY and π provide strong support for recurrent selection as the primary selective process shaping variation across pine sawfly genomes, with some contribution from balancing selection and lineage-specific linked selection. Because inheritance patterns for haplodiploid genomes are analogous to those of sex chromosomes, we hypothesize that haplodiploids may be especially prone to recurrent selection, even if gene flow occurred throughout divergence. Overall, our study helps fill an important taxonomic gap in the genomic landscape literature and contributes to our understanding of the processes that shape genome-wide patterns of genetic variation.

Geographical and ecological allopatry effects on niche change in two sister species pairs of hummingbirds in western North America

Here, we explored how variations in the allopatric speciation scenario, specifically ecological vs. vicariant allopatry, relate to climatic niche change in sister species. We selected two sister species pairs of North American hummingbirds (Calypte anna, C. costae, Basilinna leucotis, B. xantusii) that diverged 2.5 and 3.6 million years ago, under ecological (arid climate tendency during Pliocene) and vicariant (Baja California peninsula separation) allopatric processes, respectively. We constructed the climatic niche of each species using occurrence records and estimated the distance, similarity, and unique fraction of climatic niche between sister species. Calypte species showed moderate niche divergence (Euclidean distance between centroids = 1.94, Sørensen index of similarity = 0.080, unique fraction of hypervolume in C. costae = 0.57, and C. anna = 0.95). However, contrary to expectations, Basilinna species, which diverged under a vicariant scenario, displayed clear niche divergence (Euclidean distance between centroids = 3.78, Sørensen index of similarity = 0.0001, and unique fraction of hypervolume in B. xantusii = 0.98, and B. leucotis = 0.99). We explained dissimilarity in climatic niches between Basilinna species by the ecological divergence between habitats of disjunct populations, which would have also been associated with increased aridity during the Pliocene.

Viability of high-frequency environmental DNA (eDNA) sampling as a fish enumeration tool

Despite growing interest in environmental DNA (eDNA) monitoring as a low-cost, non-invasive tool for monitoring fish presence and relative abundance, quantitative comparisons between fish abundance and eDNA are still rare, especially for anadromous species of conservation concern. To examine the relationship between eDNA data and management-relevant abundance data, we assessed eDNA abundance of river herring, an ecologically relevant anadromous sister-species pair, alongside sonar-generated fish counts at a well-characterized site in the Choptank River, Chesapeake Bay, MD. Over the 2021 spawning season, there was a strong correlation between daily eDNA concentration and daily counts of fish swimming upstream (Spearman’s rho = 0.86). A generalized additive model for location scale and shape (GAMLSS) was used to estimate fish count as a function of flow-corrected eDNA concentration and relevant covariates. Model- and sonar-generated run counts were 729,385 and 733,208 fish respectively, differing by just 0.5 %. A sub-sampling analysis showed that a model built on at least five weeks of data could utilize eDNA abundance to produce accurate estimates for the remainder of the season, while a reduction in eDNA sampling frequency substantially reduced run count accuracy. This work emphasizes the utility of quantitative eDNA monitoring for river herring populations and shows the necessity of high-frequency eDNA sampling to estimate run count.

Genomic evidence reveals three W-autosome fusions in Heliconius butterflies.

Sex chromosomes are evolutionarily labile in many animals and sometimes fuse with autosomes, creating so-called neo-sex chromosomes. Fusions between sex chromosomes and autosomes have been proposed to reduce sexual conflict and to promote adaptation and reproductive isolation among species. Recently, advances in genomics have fuelled the discovery of such fusions across the tree of life. Here, we discovered multiple fusions leading to neo-sex chromosomes in the sapho subclade of the classical adaptive radiation of Heliconius butterflies. Heliconius butterflies generally have 21 chromosomes with very high synteny. However, the five Heliconius species in the sapho subclade show large variation in chromosome number ranging from 21 to 60. We find that the W chromosome is fused with chromosome 4 in all of them. Two sister species pairs show subsequent fusions between the W and chromosomes 9 or 14, respectively. These fusions between autosomes and sex chromosomes make Heliconius butterflies an ideal system for studying the role of neo-sex chromosomes in adaptive radiations and the degeneration of sex chromosomes over time. Our findings emphasize the capability of short-read resequencing to detect genomic signatures of fusion events between sex chromosomes and autosomes even when sex chromosomes are not explicitly assembled.

Climatic niche evolution and speciation modes in the transisthmian Alpheus shrimps (Caridea: Alpheidae)

AbstractAimWe studied the niche evolution and diversification modes in transisthmian Alpheus shrimps by examining the interplay between environmental niche divergence and conservatism in allopatric sister species. In a broader perspective, the current study analysed the evolution of climatic niche and the role of the environment in species diversification of Alpheus transisthmian shrimp.LocationAtlantic and Eastern‐Pacific oceans.Taxon Alpheus shrimps (Caridea: Alpheidae).MethodsWe assembled georeferenced occurrences for 33 species of Alpheus (with 24 sister species) from a time‐calibrated molecular phylogeny. We modelled their ecological niches and assessed niche overlap through pairwise comparisons. Additionally, we performed phylogenetic reconstructions of the ancestral environmental niche, for each niche axis.ResultsOur results demonstrate that thermal tolerances, food availability and hydrodynamic forces were relevant environmental axes in evolutionary processes in transisthmian species of Alpheus. Among the 528 paired comparisons, we found that most niches were divergent, including in 12 clades formed by pairs of sister species (in only two of these clades were the niches fully equivalent). Phylogenetic reconstructions of ancestral niches showed an initial niche conservatism in all axes, with divergences intensifying in the last 12 million years.Main ConclusionsWe found evidence that confirms the relevance of the environmental changes that occurred in the West Atlantic and East Pacific for niche evolution in transisthmian Alpheus species, as well as for the emergence of some lineages. Our findings provide evidence for different modes of Alpheus species speciation in a period consistent with the closure of the Isthmus of Panama.

Temperature and immune challenges modulate the transcription of genes of the ubiquitin and apoptosis pathways in two high-latitude Notothenioid fish across the Antarctic Polar Front.

Thermal variations due to global climate change are expected to modify the distributions of marine ectotherms, with potential pathogen translocations. This is of particular concern at high latitudes where cold-adapted stenothermal fish such as the Notothenioids occur. However, little is known about the combined effects of thermal fluctuations and immune challenges on the balance between cell damage and repair processes in these fish. The aim of this study was to determine the effect of thermal variation on specific genes involved in the ubiquitination and apoptosis pathways in two congeneric Notothenioid species, subjected to simulated bacterial and viral infections. Adult fish of Harpagifer bispinis and Harpagifer antarcticus were collected from Punta Arenas (Chile) and King George Island (Antarctica), respectively, and distributed as follows: injected with PBS (control), LPS (2.5mg/kg) or Poly I:C (2mg/kg) and then submitted to 2, 5 and 8°C. After 1week, samples of gills, liver and spleen were taken to evaluate the expression by real-time PCR of specific genes involved in ubiquitination (E3-ligase enzyme) and apoptosis (BAX and SMAC/DIABLO). Gene expression was tissue-dependent and increased with increasing temperature in the gills and liver while showing an opposite pattern in the spleen. Studying a pair of sister species that occur across the Antarctic Polar Front can help us understand the particular pressures of intertidal lifestyles and the effect of temperature in combination with biological stressors on cell damage and repair capacity in a changing environment.

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.

A test of trade-offs in dispersal and reproduction within and between a sister species pair of specialist insect herbivores.

Understanding the drivers of trade-offs among traits is vital for comprehending the evolution and maintenance of trait variation. Theoretical frameworks propose that evolutionary mechanisms governing trade-offs frequently exhibit a scale-dependent nature. However, empirical tests of whether trade-offs exhibited across various biological scales (i.e. individuals, populations, species, genera, etc.) remains scarce. In this study, we explore trade-off between dispersal and reproductive effort among sympatric sister species of wasps in the genus Belonocnema (Hymenoptera: Cynipini: Cynipidae) that form galls on live oaks: B. fossoria, which specializes on Quercus geminata, and B. treatae, which specializes on Q. virginiana. Specifically, our results suggest that B. fossoria has evolved reduced flight capability and smaller wings, but a larger abdomen and greater total reproductive effort than B. treatae, which has larger wings and is a stronger flier, but has a smaller abdomen and reduced total reproductive effort. These traits and the relationships among them remain unchanged when B. fossoria and B. treatae are transplanted and reared onto the alternative host plant, suggesting that trait divergence is genetically based as opposed to being a plastic response to the different rearing environments. However, when looking within species, we found no evidence of intraspecific trade-offs between wing length and reproductive traits within either B. fossoria or B. treatae. Overall, our results indicate that observed trade-offs in life history traits between the two gall former species are likely a result of independent adaptations in response to different environments as opposed to the amplified expression of within species intrinsic tradeoffs.

A comprehensive evolutionary scenario for the origin and neofunctionalization of the Drosophila speciation gene Odysseus (OdsH).

Odysseus (OdsH) was the first speciation gene described in Drosophila related to hybrid sterility in offspring of mating between Drosophila mauritiana and Drosophila simulans. Its origin is attributed to the duplication of the gene unc-4 in the subgenus Sophophora. By using a much larger sample of Drosophilidae species, we showed that contrary to what has been previously proposed, OdsH origin occurred 62 MYA. Evolutionary rates, expression, and transcription factor-binding sites of OdsH evidence that it may have rapidly experienced neofunctionalization in male sexual functions. Furthermore, the analysis of the OdsH peptide allowed the identification of mutations of D. mauritiana that could result in incompatibility in hybrids. In order to find if OdsH could be related to hybrid sterility, beyond Sophophora, we explored the expression of OdsH in Drosophila arizonae and Drosophila mojavensis, a pair of sister species with incomplete reproductive isolation. Our data indicated that OdsH expression is not atypical in their male-sterile hybrids. In conclusion, we have proposed that the origin of OdsH occurred earlier than previously proposed, followed by neofunctionalization. Our results also suggested that its role as a speciation gene might be restricted to D. mauritiana and D. simulans.

Phylogenomics of Convallarioideae (Asparagaceae), with emphasis on Vietnamese species

With the aim of inferring phylogenetic relationships among 86 species (including 45 species from Vietnam) mostly of the subfamily Convallarioideae (=Nolinoideae) (Asparagaceae sensu APG IV), we analyzed their chloroplast DNA sequences (rbcL and trnL-F) by both Bayesian inference (BI) and maximum likelihood (ML) methods. Our dataset included six of the seven tribes classified in this subfamily; Convallarieae, Dracaeneae, Liriopeae Nolineae, Polygonateae and Rusceae (Eriospermeae not examined). Our study supported the sisterhood between Convallarioideae and Asparagoideae and the monophyly of all the tribes except Polygonateae. Within the Convallarioideae we examined, Dracaena formed the basalmost clade. Theropogon did not positively nest in any of the tribes including Convallarieae in which it had often been classified. It was weakly defined as the second basalmost branch. Ruscus (Rusceae) nested in Polygonateae as the sister to Maianthemum, hence Polygonateae was recognized here as paraphyletic. Nolineae was discordant in position between BI and ML analyses, probably reflecting the limited molecular markers we examined. In both BI and ML analyses, all genera of Liriopeae and Convallarieae were monophyletic and their intergeneric relationships were consistent. In Liriopeae, Liriope was sister to the clade of Ophiopogon + Peliosanthes. In Convallarieae, Aspidistra + Tupistra formed the sister clade to Reineckea + Rohdea. Interspecific relationships within these genera were, however, not clearly resolved, except for several pairs of sister species. We also briefly discussed some of the resultant phylogenetic relationships from the morphological and/or evolutionary aspects.

Widespread sympatry in a species-rich clade of marine fishes (Carangoidei).

A universal paradigm describing patterns of speciation across the tree of life has been debated for decades. In marine organisms, inferring patterns of speciation using contemporary and historical patterns of biogeography is challenging due to the deficiency of species-level phylogenies and information on species' distributions, as well as conflicting relationships between species' dispersal, range size and co-occurrence. Most research on global patterns of marine fish speciation and biogeography has focused on coral reef or pelagic species. Carangoidei is an ecologically important clade of marine fishes that use coral reef and pelagic environments. We used sequence capture of 1314 ultraconserved elements (UCEs) from 154 taxa to generate a time-calibrated phylogeny of Carangoidei and its parent clade, Carangiformes. Age-range correlation analyses of the geographical distributions and divergence times of sister species pairs reveal widespread sympatry, with 73% of sister species pairs exhibiting sympatric geographical distributions, regardless of node age. Most species pairs coexist across large portions of their ranges. We also observe greater disparity in body length and maximum depth between sympatric relative to allopatric sister species. These and other ecological or behavioural attributes probably facilitate sympatry among the most closely related carangoids.

Evolutionary Genomics of Sister Species Differing in Effective Population Sizes and Recombination Rates.

Studies of closely related species with known ecological differences provide exceptional opportunities for understanding the genetic mechanisms of evolution. In this study, we compared population-genomics data between Daphnia pulex and Daphnia pulicaria, two reproductively compatible sister species experiencing ecological speciation, the first largely confined to intermittent ponds and the second to permanent lakes in the same geographic region. Daphnia pulicaria has lower genome-wide nucleotide diversity, a smaller effective population size, a higher incidence of private alleles, and a substantially more linkage disequilibrium than D. pulex. Positively selected genes in D. pulicaria are enriched in potentially aging-related categories such as cellular homeostasis, which may explain the extended life span in D. pulicaria. We also found that opsin-related genes, which may mediate photoperiodic responses, are under different selection pressures in these two species. Genes involved in mitochondrial functions, ribosomes, and responses to environmental stimuli are found to be under positive selection in both species. Additionally, we found that the two species have similar average evolutionary rates at the DNA-sequence level, although approximately 160 genes have significantly different rates in the two lineages. Our results provide insights into the physiological traits that differ within this regionally sympatric sister-species pair that occupies unique microhabitats.

Phylogenetics and Population Genetics of the Petrolisthes lamarckii-P. haswelli Complex in China: Old Lineage and New Species.

Petrolisthes lamarckii (Leach, 1821) and P. haswelli Miers, 1884 are a pair of sister species of porcelain crabs, both of which are common in the intertidal zone of southern China, typically found under rocks and in the crevices of coral reefs. However, the distribution, genetic relationship and diversity of the two species in China have not been rigorously studied. Meanwhile, P. lamarckii is considered as a complex of cryptic species due to their diverse morphological features. In this study, we identified 127 specimens of the P. lamarckii-P. haswelli complex (LH complex) and recognised a new species through morphological and molecular analysis. Furthermore, we constructed a time-calibrated phylogeny of the LH complex using three mitochondrial and two nuclear genes from all three species, finding that the divergence of the LH complex can be traced back to the Miocene epoch, and that the genetic diversity increased during the Mid-Pleistocene transition period. Glacial refugia formed during the Pleistocene climatic oscillations has been regarded as one of the contributing factors to the diversification of marine organisms in the north-western Pacific. Petrolisthes haswelli demonstrates a wide distribution along the southern coast of China, while other lineages display more restricted distributions. The research on the demographic history and gene flow of P. haswelli revealed that the Chinese coastal populations experienced an expansion event approximately 12.5 thousand years ago (Kya) and the asymmetrical gene flows were observed between the two sides of the Taiwan Strait and Qiongzhou Strait, respectively, which is likely influenced by the restriction of ocean currents.

Demographically explicit scans for barriers to gene flow using gIMble.

Identifying regions of the genome that act as barriers to gene flow between recently diverged taxa has remained challenging given the many evolutionary forces that generate variation in genetic diversity and divergence along the genome, and the stochastic nature of this variation. Progress has been impeded by a conceptual and methodological divide between analyses that infer the demographic history of speciation and genome scans aimed at identifying locally maladaptive alleles i.e. genomic barriers to gene flow. Here we implement genomewide IM blockwise likelihood estimation (gIMble), a composite likelihood approach for the quantification of barriers, that bridges this divide. This analytic framework captures background selection and selection against barriers in a model of isolation with migration (IM) as heterogeneity in effective population size (Ne) and effective migration rate (me), respectively. Variation in both effective demographic parameters is estimated in sliding windows via pre-computed likelihood grids. gIMble includes modules for pre-processing/filtering of genomic data and performing parametric bootstraps using coalescent simulations. To demonstrate the new approach, we analyse data from a well-studied pair of sister species of tropical butterflies with a known history of post-divergence gene flow: Heliconius melpomene and H. cydno. Our analyses uncover both large-effect barrier loci (including well-known wing-pattern genes) and a genome-wide signal of a polygenic barrier architecture.

Integrative taxonomy reveals unrecognised species diversity in African Corypha larks (Aves: Alaudidae)

Abstract The species complex comprising the rufous-naped lark Corypha africana, Sharpe’s lark Corypha sharpii, the red-winged lark Corypha hypermetra, the Somali long-billed lark Corypha somalica and Ash’s lark Corypha ashi encompasses 31 recognised taxa across sub-Saharan Africa, many of which are extremely poorly known and some not observed for decades. Only 17 taxa have been studied molecularly and none comprehensively for morphology, vocalisations or other behaviours. Here, we undertake comprehensive integrative taxonomic analyses based on plumage and morphometrics (for 97% of the taxa), mitochondrial and nuclear loci (77%), ≤ 1.3 million genome-wide single nucleotide polymorphisms (68%), song (many described for the first time; 52%) and additional behavioural data (45%). All polytypic species as presently circumscribed are paraphyletic, with eight primary clades separated by ≤ 6.3–6.8 Myr, broadly supported by plumage, morphometrics, song and other behaviours. The most recent divergences concern sympatric taxon pairs usually treated as separate species, whereas the divergence of all clades including C. africana subspecies is as old as sister species pairs in other lark genera. We propose the recognition of nine instead of five species, while C. ashi is synonymised with C. somalica rochei as C. s. ashi. The geographical distributions are incompletely known, and although the nine species are generally para-/allopatric, some might be sympatric.

Geographical and ecological drivers of coexistence dynamics in squamate reptiles

AbstractAimSpecies richness varies widely across space and is determined by underlying factors that drive species coexistence. Such factors include the speciation process (sympatric vs. allopatric), time since divergence, geographic context and intrinsic properties of the organisms. We model for the first time the coexistence dynamics of lizards and snakes across broad temporal and spatial scales, investigating whether an increase in niche divergence, dispersal abilities and inhabiting islands or continents affect their probability of coexistence.LocationGlobal.Time periodCenozoic.Major taxa studiedSquamata.MethodsWe used 447 sister species pairs, their age since divergence, their level of spatial (sympatric or allopatric) and niche overlap and geographical setting (islands or continents) to fit probabilistic models of species coexistence. We measured morphological traits to quantify niche divergence and used range and body size as proxies for dispersal ability. We applied a model‐comparison framework in lizards and snakes separately to evaluate which factors best explained their coexistence dynamics.ResultsAllopatric speciation is the main speciation mode in snakes but we did not find evidence to favour one speciation mode in lizards. In snakes, sympatric pairs tend to occur on islands and to be more different in body size. On the contrary, dispersal ability shaped the coexistence of lizards, where species were more likely to coexist when they have higher dispersal abilities.Main conclusionsDistinct patterns and mechanisms underlie species coexistence within the order Squamata. Snake coexistence is preferentially produced by secondary sympatry favoured by niche divergence and is more likely to occur in more restricted geographical settings (islands vs. continents). Coexistence in lizards is strongly influenced only by dispersal abilities, but the high heterogeneity of processes simultaneously shaping the distribution of different lizard lineages might have masked specific coexistence signals, and future work should compare coexistence dynamics between clades (e.g. families).

Host shift promotes divergent evolution between closely related holoparasitic species

Distinct hosts have been hypothesized to possess the potential for affecting species differentiation and genome evolution of parasitic organisms. However, what host shift history is experienced by the closely related parasites and whether disparate evolution of their genomes occur remain largely unknown. Here, we screened horizontal gene transfer (HGT) events in a pair of sister species of holoparasitic Boschniakia (Orobanchaceae) having obligate hosts from distinct families to recall the former host-parasite associations and performed a comparative analysis to investigate the difference of their organelle genomes. Except those from the current hosts (Ericaceae and Betulaceae), we identified a number of HGTs from Rosaceae supporting the occurrence of unexpected ancient host shifts. Different hosts transfer functional genes which changed nuclear genomes of this sister species. Likewise, different donors transferred sequences to their mitogenomes, which vary in size due to foreign and repetitive elements rather than other factors found in other parasites. The plastomes are both severely reduced, and the degree of difference in reduction syndrome reaches the intergeneric level. Our findings provide new insights into the genome evolution of parasites adapting to different hosts and extend the mechanism of host shift promoting species differentiation to parasitic plant lineages.

Allopatric speciation is more prevalent than parapatric ecological divergence in a recent high-Andean diversification (Linochilus: Asteraceae).

Elucidating how species accumulate in diversity hotspots is an ongoing debate in evolutionary biology. The páramo, in the Northern Andes, has remarkably high indices of plant diversity, endemicity, and diversification rates. A hypothesis for explaining such indices is that allopatric speciation is high in the páramo given its island-like distribution. An alternative hypothesis is that the altitudinal gradient of the Andean topography provides a variety of niches that drive vertical parapatric ecological speciation. A formal test for evaluating the relative roles of allopatric and parapatric ecological speciation is lacking. The main aim of our study is to test which kind of speciation is more common in an endemic páramo genus. We developed a framework incorporating phylogenetics, species' distributions, and a morpho-ecological trait (leaf area) to compare sister species and infer whether allopatric or parapatric ecological divergence caused their speciation. We applied our framework to the species-rich genus Linochilus (63 spp.) and found that the majority of recent speciation events in it (12 events, 80%) have been driven by allopatric speciation, while a smaller fraction (one event, 6.7%) is attributed to parapatric ecological speciation; two pairs of sister species produced inconclusive results (13.3%). We conclude that páramo autochthonous (in-situ) diversification has been primarily driven by allopatric speciation.

Lacustrine speciation associated with chromosomal inversion in a lineage of riverine fishes.

Geographic isolation is the primary driver of speciation in many vertebrate lineages. This trend is exemplified by North American darters, a clade of freshwater fishes where nearly all sister species pairs are allopatric and separated by millions of years of divergence. One of the only exceptions is the Lake Waccamaw endemic Etheostoma perlongum and its riverine sister species Etheostoma maculaticeps, which have no physical barriers to gene flow. Here we show that lacustrine speciation of E. perlongum is characterized by morphological and ecological divergence likely facilitated by a large chromosomal inversion. While E. perlongum is phylogenetically nested within the geographically widespread E. maculaticeps, there is a sharp genetic and morphological break coinciding with the lake-river boundary in the Waccamaw River system. Despite recent divergence, an active hybrid zone, and ongoing gene flow, analyses using a de novo reference genome reveal a 9 Mb chromosomal inversion with elevated divergence between E. perlongum and E. maculaticeps. This region exhibits striking synteny with known inversion supergenes in two distantly related fish lineages, suggesting deep evolutionary convergence of genomic architecture. Our results illustrate that rapid, ecological speciation with gene flow is possible even in lineages where geographic isolation is the dominant mechanism of speciation.

The role of climate change and niche shifts in divergent range dynamics of a sister-species pair.

Species ranges are set by limitations in factors including climate tolerances, habitat use, and dispersal abilities. Understanding the factors governing species range dynamics remains a challenge that is ever more important in our rapidly changing world. Species ranges can shift if environmental changes affect available habitat, or if the niche or habitat connectivity of a species changes. We tested how changes in habitat availability, niche, or habitat connectivity could contribute to divergent range dynamics in a sister-species pair. The great-tailed grackle (Quiscalus mexicanus) has expanded its range northward from Texas to Nebraska in the past 40 years, while its closest relative, the boattailed grackle (Quiscalus major), has remained tied to the coasts of the Atlantic Ocean and the Gulf of Mexico as well as the interior of Florida. We created species distribution and connectivity models trained on citizen science data from 1970-1979 and 2010-2019 to determine how the availability of habitat, the types of habitat occupied, and range-wide connectivity have changed for both species. We found that the two species occupy distinct habitats and that the great-tailed grackle has shifted to occupy a larger breadth of urban, arid environments farther from natural water sources. Meanwhile, the boattailed grackle has remained limited to warm, wet, coastal environments. We found no evidence that changes in habitat connectivity affected the ranges of either species. Overall, our results suggest that the great-tailed grackle has shifted its realized niche as part of its rapid range expansion, while the range dynamics of the boat-tailed grackle may be shaped more by climate change. The expansion in habitats occupied by the great-tailed grackle is consistent with observations that species with high behavioral flexibility can rapidly expand their geographic range by using human-altered habitat. This investigation identifies how opposite responses to anthropogenic change could drive divergent range dynamics, elucidating the factors that have and will continue to shape species ranges.