Senckenbergische Naturforschende Gesellschaft
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Bird-mediated seed dispersal is crucial for the regeneration and viability of ecosystems, often resulting in complex mutualistic species networks. Yet, how this mutualism drives the evolution of seed dispersing birds is still poorly understood. In the present study we combine whole genome re-sequencing analyses and morphometric data to assess the evolutionary processes that shaped the diversification of the Eurasian nutcracker (Nucifraga), a seed disperser known for its mutualism with pines (Pinus). Our results show that the divergence and phylogeographic patterns of nutcrackers resemble those of other non-mutualistic passerine birds and suggest that their early diversification was shaped by similar biogeographic and climatic processes. The limited variation in foraging traits indicates that local adaptation to pines likely played a minor role. Our study shows that close mutualistic relationships between bird and plant species might not necessarily act as a primary driver of evolution and diversification in resource-specialized birds.
Background: Genome sequencing of all known eukaryotes on Earth promises unprecedented advances in biological sciences and in biodiversity-related applied fields such as environmental management and natural product research. Advances in long-read DNA sequencing make it feasible to generate high-quality genomes for many non–genetic model species. However, long-read sequencing today relies on sizable quantities of high-quality, high molecular weight DNA, which is mostly obtained from fresh tissues. This is a challenge for biodiversity genomics of most metazoan species, which are tiny and need to be preserved immediately after collection. Here we present de novo genomes of 2 species of submillimeter Collembola. For each, we prepared the sequencing library from high molecular weight DNA extracted from a single specimen and using a novel ultra-low input protocol from Pacific Biosciences. This protocol requires a DNA input of only 5 ng, permitted by a whole-genome amplification step.
Results: The 2 assembled genomes have N50 values >5.5 and 8.5 Mb, respectively, and both contain ∼96% of BUSCO genes. Thus, they are highly contiguous and complete. The genomes are supported by an integrative taxonomy approach including placement in a genome-based phylogeny of Collembola and designation of a neotype for 1 of the species. Higher heterozygosity values are recorded in the more mobile species. Both species are devoid of the biosynthetic pathway for β-lactam antibiotics known in several Collembola, confirming the tight correlation of antibiotic synthesis with the species way of life.
Conclusions: It is now possible to generate high-quality genomes from single specimens of minute, field-preserved metazoans, exceeding the minimum contig N50 (1 Mb) required by the Earth BioGenome Project.
The snake pipefish, Entelurus aequoreus (Linnaeus, 1758), is a slender, up to 60 cm long, northern Atlantic fish that dwells in open seagrass habitats and has recently expanded its distribution range. The snake pipefish is part of the family Syngnathidae (seahorses and pipefish) that has undergone several characteristic morphological changes, such as loss of pelvic fins and elongated snout. Here, we present a highly contiguous, near chromosome-scale genome of the snake pipefish assembled as part of a university master’s course. The final assembly has a length of 1.6 Gbp in 7,391 scaffolds, a scaffold and contig N50 of 62.3 Mbp and 45.0 Mbp and L50 of 12 and 14, respectively. The largest 28 scaffolds (>21 Mbp) span 89.7% of the assembly length. A BUSCO completeness score of 94.1% and a mapping rate above 98% suggest a high assembly completeness. Repetitive elements cover 74.93% of the genome, one of the highest proportions so far identified in vertebrate genomes. Demographic modeling using the PSMC framework indicates a peak in effective population size (50 – 100 kya) during the last interglacial period and suggests that the species might largely benefit from warmer water conditions, as seen today. Our updated snake pipefish assembly forms an important foundation for further analysis of the morphological and molecular changes unique to the family Syngnathidae.
Highlights
• Genomes for all five Natrix species, two represented by two distinct subspecies each, were sequenced.
• Two genomes were de-novo assembled to their 1.7 Gb length with a contig N50 of 4.6 Mbp and 1.5 Mbp.
• Evidence for interspecific hybridization, both between allopatric and widely sympatric species.
• Fossil-calibrated molecular clock using genomes indicates that species are ancient several million-year-old lineages.
• Our findings imply that speciation took place despite continued gene flow.
Abstract
Understanding speciation is one of the cornerstones of biological diversity research. Currently, speciation is often understood as a continuous process of divergence that continues until genetic or other incompatibilities minimize or prevent interbreeding. The Palearctic snake genus Natrix is an ideal group to study speciation, as it comprises taxa representing distinct stages of the speciation process, ranging from widely interbreeding parapatric taxa through parapatric species with very limited gene flow in narrow hybrid zones to widely sympatric species. To understand the evolution of reproductive isolation through time, we have sequenced the genomes of all five species within this genus and two additional subspecies. We used both long-read and short-read methods to sequence and de-novo-assemble two high-quality genomes (Natrix h. helvetica, Natrix n. natrix) to their 1.7 Gb length with a contig N50 of 4.6 Mbp and 1.5 Mbp, respectively, and used these as references to assemble the remaining short-read-based genomes. Our phylogenomic analyses yielded a well-supported dated phylogeny and evidence for a surprisingly complex history of interspecific gene flow, including between widely sympatric species. Furthermore, evidence for gene flow was also found for currently allopatric species pairs. Genetic exchange among these well-defined, distinct, and several million-year-old reptile species emphasizes that speciation and maintenance of species distinctness can occur despite continued genetic exchange.
Background: In the speciation continuum, the strength of reproductive isolation varies, and species boundaries are blurred by gene flow. Interbreeding among giraffe (Giraffa spp.) in captivity is known, and anecdotal reports of natural hybrids exist. In Kenya, Nubian (G. camelopardalis camelopardalis), reticulated (G. reticulata), and Masai giraffe sensu stricto (G. tippelskirchi tippelskirchi) are parapatric, and thus, the country might be a melting pot for these taxa. We analyzed 128 genomes of wild giraffe, 113 newly sequenced, representing these three taxa.
Results: We found varying levels of Nubian ancestry in 13 reticulated giraffe sampled across the Laikipia Plateau most likely reflecting historical gene flow between these two lineages. Although comparatively weaker signs of ancestral gene flow and potential mitochondrial introgression from reticulated into Masai giraffe were also detected, estimated admixture levels between these two lineages are minimal. Importantly, contemporary gene flow between East African giraffe lineages was not statistically significant. Effective population sizes have declined since the Late Pleistocene, more severely for Nubian and reticulated giraffe.
Conclusions: Despite historically hybridizing, these three giraffe lineages have maintained their overall genomic integrity suggesting effective reproductive isolation, consistent with the previous classification of giraffe into four species.
Background: In the speciation continuum the strength of reproductive isolation varies, and species boundaries are blurred by gene flow. Interbreeding among giraffe (Giraffa spp.) in captivity is known and anecdotal reports of natural hybrids exist. In Kenya, Nubian (G. camelopardalis camelopardalis), reticulated (G. reticulata), and Masai giraffe sensu stricto (G. tippelskirchi tippelskirchi) are parapatric, and thus the country might be a melting pot for these taxa. We analyzed 128 genomes of wild giraffe, 113 newly sequenced, representing these three taxa.
Results: We found varying levels of Nubian ancestry in 13 reticulated giraffe sampled across the Laikipia Plateau most likely reflecting historical gene flow between these two lineages. Although comparatively weaker signs of ancestral gene flow and potential mitochondrial introgression from reticulated into Masai giraffe were also detected, estimated admixture levels between these two lineages are minimal. Importantly, contemporary gene flow between East African giraffe lineages was not statistically significant. Effective population sizes have declined since the Late Pleistocene, more severely for Nubian and reticulated giraffe.
Conclusions: Despite historically hybridizing, these three giraffe lineages have maintained their overall genomic integrity suggesting effective reproductive isolation, consistent with the previous classification of giraffe into four species.
Three of the four species of giraffe are threatened, particularly the northern giraffe (Giraffa camelopardalis), which collectively have the smallest known wild population estimates. Among the three subspecies of the northern giraffe, the West African giraffe (Giraffa camelopardalis peralta) had declined to 49 individuals by 1996 and only recovered due to conservation efforts undertaken in the past 25 years, while the Kordofan giraffe (Giraffa camelopardalis antiquorum) remains at <2300 individuals distributed in small, isolated populations over a large geographical range in Central Africa. These combined factors could lead to genetically depauperated populations. We analyzed 119 mitochondrial sequences and 26 whole genomes of northern giraffe individuals to investigate their population structure and assess the recent demographic history and current genomic diversity of West African and Kordofan giraffe. Phylogenetic and population structure analyses separate the three subspecies of northern giraffe and suggest genetic differentiation between populations from eastern and western areas of the Kordofan giraffe’s range. Both West African and Kordofan giraffe show a gradual decline in effective population size over the last 10 ka and have moderate genome-wide heterozygosity compared to other giraffe species. Recent inbreeding levels are higher in the West African giraffe and in Kordofan giraffe from Garamba National Park, Democratic Republic of Congo. Although numbers for both West African and some populations of Kordofan giraffe have increased in recent years, the threat of habitat loss, climate change impacts, and illegal hunting persists. Thus, future conservation actions should consider close genetic monitoring of populations to detect and, where practical, counteract negative trends that might develop.
Bears are iconic mammals with a complex evolutionary history. Natural bear hybrids and studies of few nuclear genes indicate that gene flow among bears may be more common than expected and not limited to the closely related polar and brown bears. Here we present a genome analysis of the bear family with representatives of all living species. Phylogenomic analyses of 869 mega base pairs divided into 18,621 genome fragments yielded a well-resolved coalescent species tree despite signals for extensive gene flow across species. However, genome analyses using three different statistical methods show that gene flow is not limited to closely related species pairs. Strong ancestral gene flow between the Asiatic black bear and the ancestor to polar, brown and American black bear explains numerous uncertainties in reconstructing the bear phylogeny. Gene flow across the bear clade may be mediated by intermediate species such as the geographically wide-spread brown bears leading to massive amounts of phylogenetic conflict. Genome-scale analyses lead to a more complete understanding of complex evolutionary processes. The increasing evidence for extensive inter-specific gene flow, found also in other animal species, necessitates shifting the attention from speciation processes achieving genome-wide reproductive isolation to the selective processes that maintain species divergence in the face of gene flow.
All giraffe (Giraffa) were previously assigned to a single species (G. Camelopardalis) and nine subspecies. However, multi-locus analyses of all subspecies have shown that there are four genetically distinct clades and suggest four giraffe species. This conclusion might not be fully accepted due to limited data and lack of explicit gene flow analyses. Here we present an extended study based on 21 independent nuclear loci from 137 individuals. Explicit gene flow analyses identify less than one migrant per generation, including between the closely related northern and reticulated giraffe. Thus, gene flow analyses and population genetics of the extended dataset confirm four genetically distinct giraffe clades and support four independent giraffe species. The new findings call for a revision of the IUCN classification of giraffe taxonomy. Three of the four species are threatened with extinction, mostly occurring in politically unstable regions, and as such, require the highest conservation support possible.
Species is the fundamental taxonomic unit in biology and its delimitation has implications for conservation. In giraffe (Giraffa spp.), multiple taxonomic classifications have been proposed since the early 1900s.1 However, one species with nine subspecies has been generally accepted,2 likely due to limited in-depth assessments, subspecies hybridizing in captivity,3,4 and anecdotal reports of hybrids in the wild.5 Giraffe taxonomy received new attention after population genetic studies using traditional genetic markers suggested at least four species.6,7 This view has been met with controversy,8 setting the stage for debate.9,10 Genomics is significantly enhancing our understanding of biodiversity and speciation relative to traditional genetic approaches and thus has important implications for species delineation and conservation.11 We present a high-quality de novo genome assembly of the critically endangered Kordofan giraffe (G. camelopardalis antiquorum)12 and a comprehensive whole-genome analysis of 50 giraffe representing all traditionally recognized subspecies. Population structure and phylogenomic analyses support four separately evolving giraffe lineages, which diverged 230–370 ka ago. These lineages underwent distinct demographic histories and show different levels of heterozygosity and inbreeding. Our results strengthen previous findings of limited gene flow and admixture among putative giraffe species6,7,9 and establish a genomic foundation for recognizing four species and seven subspecies, the latter of which should be considered as evolutionary significant units. Achieving a consensus over the number of species and subspecies in giraffe is essential for adequately assessing their threat level and will improve conservation efforts for these iconic taxa.