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Genetic divergence is impacted by many factors, including phylogenetic history, gene flow, genetic drift, and divergent selection. Rotifers are an important component of aquatic ecosystems, and genetic variation is essential to their ongoing adaptive diversification and local adaptation. In addition to coding sequence divergence, variation in gene expression may relate to variable heat tolerance, and can impose ecological barriers within species. Temperature plays a significant role in aquatic ecosystems by affecting species abundance, spatio-temporal distribution, and habitat colonization. Recently described (formerly cryptic) species of the Brachionus calyciflorus complex exhibit different temperature tolerance both in natural and in laboratory studies, and show that B. calyciflorus sensu stricto (s.s.) is a thermotolerant species. Even within B. calyciflorus s.s., there is a tendency for further temperature specializations. Comparison of expressed genes allows us to assess the impact of stressors on both expression and sequence divergence among disparate populations within a single species. Here, we have used RNA-seq to explore expressed genetic diversity in B. calyciflorus s.s. in two mitochondrial DNA lineages with different phylogenetic histories and differences in thermotolerance. We identify a suite of candidate genes that may underlie local adaptation, with a particular focus on the response to sustained high or low temperatures. We do not find adaptive divergence in established candidate genes for thermal adaptation. Rather, we detect divergent selection among our two lineages in genes related to metabolism (lipid metabolism, metabolism of xenobiotics).
Genetic divergence and the frequency of hybridization are central for defining species delimitations, especially among cryptic species where morphological differences are merely absent. Rotifers are known for their high cryptic diversity and therefore are ideal model organisms to investigate such patterns. Here, we used the recently resolved Brachionus calyciflorus species complex to investigate whether previously observed between species differences in thermotolerance and gene expression are also reflected in their genomic footprint. We identified a Heat Shock Protein gene (HSP 40 kDa) which exhibits cross species pronounced sequence variation. This gene exhibits species-specific fixed sites, alleles, and sites putatively under positive selection. These sites are located in protein binding regions involved in chaperoning and may therefore reflect adaptive diversification. By comparing three genetic markers (ITS, COI, HSP 40 kDa), we revealed hybridization events between the cryptic species. The low frequency of introgressive haplotypes/alleles suggest a tight, but not fully impermeable boundary between the cryptic species.
Abstract
Background
The unisexual Amazon molly (Poecilia formosa) originated from a hybridization between two sexual species, the sailfin molly (Poecilia latipinna) and the Atlantic molly (Poecilia mexicana). The Amazon molly reproduces clonally via sperm-dependent parthenogenesis (gynogenesis), in which the sperm of closely related species triggers embryogenesis of the apomictic oocytes, but typically does not contribute genetic material to the next generation. We compare for the first time the gonadal transcriptome of the Amazon molly to those of both ancestral species, P. mexicana and P. latipinna.
Results
We sequenced the gonadal transcriptomes of the P. formosa and its parental species P. mexicana and P. latipinna using Illumina RNA-sequencing techniques (paired-end, 100 bp). De novo assembly of about 50 million raw read pairs for each species was performed using Trinity, yielding 106,922 transcripts for P. formosa, 115,175 for P. latipinna, and 133,025 for P. mexicana after eliminating contaminations. On the basis of sequence similarity comparisons to other teleost species and the UniProt databases, functional annotation, and differential expression analysis, we demonstrate the similarity of the transcriptomes among the three species. More than 40% of the transcripts for each species were functionally annotated and about 70% were assigned to orthologous genes of a closely related species. Differential expression analysis between the sexual and unisexual species uncovered 2035 up-regulated and 564 down-regulated genes in P. formosa. This was exemplary validated for six genes by qRT-PCR.
Conclusions
We identified more than 130 genes related to meiosis and reproduction within the apomictically reproducing P. formosa. Overall expression of these genes seems to be down-regulated in the P. formosa transcriptome compared to both ancestral species (i.e., 106 genes down-regulated, 29 up-regulated). A further 35 meiosis and reproduction related genes were not found in the P. formosa transcriptome, but were only expressed in the sexual species. Our data support the hypothesis of general down-regulation of meiosis-related genes in the apomictic Amazon molly. Furthermore, the obtained dataset and identified gene catalog will serve as a resource for future research on the molecular mechanisms behind the reproductive mode of this unisexual species.
The complete mitochondrial genome of a European fire-bellied toad (Bombina bombina) from Germany
(2019)
The European fire-bellied toad, Bombina bombina, is a small aquatic toad belonging to the family Bombinatoridae. The species is native to the lowlands of Central and Eastern Europe, where population numbers have been in decline in recent past decades. Here, we present the first complete mitochondrial genome of the endangered European fire-bellied toad from Northern Germany recovered using iterative mapping. Phylogenetic analyses including other representatives of the Bombinatoridae placed our German specimen as sister to a Polish B. bombina sequence with high support. This finding is congruent with the postulated Pleistocene history of the species. Our complete mitochondrial genome represents an important resource for further population analysis of the European fire-bellied toad, especially those found within Germany.
Changes in species' distributions are classically projected based on their climate envelopes. For Siberian forests, which have a tremendous significance for vegetation-climate feedbacks, this implies future shifts of each of the forest-forming larch (Larix) species to the north-east. However, in addition to abiotic factors, reliable projections must assess the role of historical biogeography and biotic interactions. Here, we use sedimentary ancient DNA and individual-based modelling to investigate the distribution of larch species and mitochondrial haplotypes through space and time across the treeline ecotone on the southern Taymyr peninsula, which at the same time presents a boundary area of two larch species. We find spatial and temporal patterns, which suggest that forest density is the most influential driver determining the precise distribution of species and mitochondrial haplotypes. This suggests a strong influence of competition on the species' range shifts. These findings imply possible climate change outcomes that are directly opposed to projections based purely on climate envelopes. Investigations of such fine-scale processes of biodiversity change through time are possible using paleoenvironmental DNA, which is available much more readily than visible fossils and can provide information at a level of resolution that is not reached in classical palaeoecology.
Thermal stress response is an essential physiological trait that determines occurrence and temporal succession in nature, including response to climate change. We compared temperature-related demography in closely related heat-tolerant and heat-sensitive Brachionus rotifer species. We found significant differences in heat response, with the heat-sensitive species adopting a strategy of long survival and low population growth, while the heat-tolerant followed the opposite strategy. In both species, we examined the genetic basis of physiological variation by comparing gene expression across increasing temperatures. Comparative transcriptomic analyses identified shared and opposing responses to heat. Interestingly, expression of heat shock proteins (hsps) was strikingly different in the two species and mirrored differences in population growth rates, showing that hsp genes are likely a key component of a species’ adaptation to different temperatures. Temperature induction caused opposing patterns of expression in further functional categories including energy, carbohydrate and lipid metabolism, and in genes related to ribosomal proteins. In the heat-sensitive species, elevated temperatures caused up-regulation of genes related to meiosis induction and post-translational histone modifications. This work demonstrates the sweeping reorganizations of biological functions that accompany temperature adaptation in these two species and reveals potential molecular mechanisms that might be activated for adaptation to global warming.
Spotlight on islands
(2018)
Groups of proximate continental islands may conceal more tangled phylogeographic patterns than oceanic archipelagos as a consequence of repeated sea level changes, which allow populations to experience gene flow during periods of low sea level stands and isolation by vicariant mechanisms during periods of high sea level stands. Here, we describe for the first time an ancient and diverging lineage of the Italian wall lizard Podarcis siculus from the western Pontine Islands. We used nuclear and mitochondrial DNA sequences of 156 individuals with the aim of unraveling their phylogenetic position, while microsatellite loci were used to test several a priori insular biogeographic models of migration with empirical data. Our results suggest that the western Pontine populations colonized the islands early during their Pliocene volcanic formation, while populations from the eastern Pontine Islands seem to have been introduced recently. The inter-island genetic makeup indicates an important role of historical migration, probably due to glacial land bridges connecting islands followed by a recent vicariant mechanism of isolation. Moreover, the most supported migration model predicted higher gene flow among islands which are geographically arranged in parallel. Considering the threatened status of small insular endemic populations, we suggest this new evolutionarily independent unit be given priority in conservation efforts.
The population structure of the highly mobile marine mammal, the harbor porpoise (Phocoena phocoena), in the Atlantic shelf waters follows a pattern of significant isolation-by-distance. The population structure of harbor porpoises from the Baltic Sea, which is connected with the North Sea through a series of basins separated by shallow underwater ridges, however, is more complex. Here, we investigated the population differentiation of harbor porpoises in European Seas with a special focus on the Baltic Sea and adjacent waters, using a population genomics approach. We used 2872 single nucleotide polymorphisms (SNPs), derived from double digest restriction-site associated DNA sequencing (ddRAD-seq), as well as 13 microsatellite loci and mitochondrial haplotypes for the same set of individuals. Spatial principal components analysis (sPCA), and Bayesian clustering on a subset of SNPs suggest three main groupings at the level of all studied regions: the Black Sea, the North Atlantic, and the Baltic Sea. Furthermore, we observed a distinct separation of the North Sea harbor porpoises from the Baltic Sea populations, and identified splits between porpoise populations within the Baltic Sea. We observed a notable distinction between the Belt Sea and the Inner Baltic Sea sub-regions. Improved delineation of harbor porpoise population assignments for the Baltic based on genomic evidence is important for conservation management of this endangered cetacean in threatened habitats, particularly in the Baltic Sea proper. In addition, we show that SNPs outperform microsatellite markers and demonstrate the utility of RAD-tags from a relatively small, opportunistically sampled cetacean sample set for population diversity and divergence analysis.
Northern range margin populations of the European fire-bellied toad (Bombina bombina) have rapidly declined during recent decades. Extensive agricultural land use has fragmented the landscape, leading to habitat disruption and loss, as well as eutrophication of ponds. In Northern Germany (Schleswig-Holstein) and Southern Sweden (Skåne), this population decline resulted in decreased gene flow from surrounding populations, low genetic diversity, and a putative reduction in adaptive potential, leaving populations vulnerable to future environmental and climatic changes. Previous studies using mitochondrial control region and nuclear transcriptome-wide SNP data detected introgressive hybridization in multiple northern B. bombina populations after unreported release of toads from Austria. Here, we determine the impact of this introgression by comparing the body conditions (proxy for fitness) of introgressed and nonintrogressed populations and the genetic consequences in two candidate genes for putative local adaptation (the MHC II gene as part of the adaptive immune system and the stress response gene HSP70 kDa). We detected regional differences in body condition and observed significantly elevated levels of within individual MHC allele counts in introgressed Swedish populations, associated with a tendency toward higher body weight, relative to regional nonintrogressed populations. These differences were not observed among introgressed and nonintrogressed German populations. Genetic diversity in both MHC and HSP was generally lower in northern than Austrian populations. Our study sheds light on the potential benefits of translocations of more distantly related conspecifics as a means to increase adaptive genetic variability and fitness of genetically depauperate range margin populations without distortion of local adaptation.
The all-female Amazon molly (Poecilia formosa) originated from a single hybridization of two bisexual ancestors, Atlantic molly (Poecilia mexicana) and sailfin molly (Poecilia latipinna). As a gynogenetic species, the Amazon molly needs to copulate with a heterospecific male, but the genetic information of the sperm-donor does not contribute to the next generation, as the sperm only acts as the trigger for the diploid eggs’ embryogenesis. Here, we study the sequence evolution and gene expression of the duplicated genes coding for androgen receptors (ars) and other pathway-related genes, i.e., the estrogen receptors (ers) and cytochrome P450, family19, subfamily A, aromatase genes (cyp19as), in the Amazon molly, in comparison to its bisexual ancestors. Mollies possess–as most other teleost fish—two copies of the ar, er, and cyp19a genes, i.e., arα/arβ, erα/erβ1, and cyp19a1 (also referred as cyp19a1a)/cyp19a2 (also referred to as cyp19a1b), respectively. Non-synonymous single nucleotide polymorphisms (SNPs) among the ancestral bisexual species were generally predicted not to alter protein function. Some derived substitutions in the P. mexicana and one in P. formosa are predicted to impact protein function. We also describe the gene expression pattern of the ars and pathway-related genes in various tissues (i.e., brain, gill, and ovary) and provide SNP markers for allele specific expression research. As a general tendency, the levels of gene expression were lowest in gill and highest in ovarian tissues, while expression levels in the brain were intermediate in most cases. Expression levels in P. formosa were conserved where expression did not differ between the two bisexual ancestors. In those cases where gene expression levels significantly differed between the bisexual species, P. formosa expression was always comparable to the higher expression level among the two ancestors. Interestingly, erβ1 was expressed neither in brain nor in gill in the analyzed three molly species, which implies a more important role of erα in the estradiol synthesis pathway in these tissues. Furthermore, our data suggest that interactions of steroid-signaling pathway genes differ across tissues, in particular the interactions of ars and cyp19as.