Dataset Information

Hierarchical Hybrid Enrichment: Multitiered Genomic Data Collection Across Evolutionary Scales, With Application to Chorus Frogs (Pseudacris).

ABSTRACT: Determining the optimal targets of genomic subsampling for phylogenomics, phylogeography, and population genomics remains a challenge for evolutionary biologists. Of the available methods for subsampling the genome, hybrid enrichment (sequence capture) has become one of the primary means of data collection for systematics, due to the flexibility and cost efficiency of this approach. Despite the utility of this method, information is lacking as to what genomic targets are most appropriate for addressing questions at different evolutionary scales. In this study, first, we compare the benefits of target loci developed for deep- and shallow scales by comparing these loci at each of three taxonomic levels: within a genus (phylogenetics), within a species (phylogeography), and within a hybrid zone (population genomics). Specifically, we target evolutionarily conserved loci that are appropriate for deeper phylogenetic scales and more rapidly evolving loci that are informative for phylogeographic and population genomic scales. Second, we assess the efficacy of targeting multiple-locus sets for different taxonomic levels in the same hybrid enrichment reaction, an approach we term hierarchical hybrid enrichment. Third, we apply this approach to the North American chorus frog genus Pseudacris to answer key evolutionary questions across taxonomic and temporal scales. We demonstrate that in this system the type of genomic target that produces the most resolved gene trees differs depending on the taxonomic level, although the potential for error is substantially lower for the deep-scale loci at all levels. We successfully recover data for the two different locus sets with high efficiency. Using hierarchical data targeting deep and shallow levels: we 1) resolve the phylogeny of the genus Pseudacris and introduce a novel visual and hypothesis testing method that uses nodal heat maps to examine the robustness of branch support values to the removal of sites and loci; 2) estimate the phylogeographic history of Pseudacris feriarum, which reveals up to five independent invasions leading to sympatry with congener Pseudacris nigrita to form replicated reinforcement contact zones with ongoing gene flow into sympatry; and 3) quantify with high confidence the frequency of hybridization in one of these zones between P. feriarum and P. nigrita, which is lower than microsatellite-based estimates. We find that the hierarchical hybrid enrichment approach offers an efficient, multitiered data collection method for simultaneously addressing questions spanning multiple evolutionary scales. [Anchored hybrid enrichment; heat map; hybridization; phylogenetics; phylogeography; population genomics; reinforcement; reproductive character displacement.].

SUBMITTER: Banker SE

PROVIDER: S-EPMC7302053 | biostudies-literature | 2020 Jul

REPOSITORIES: biostudies-literature

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Hierarchical Hybrid Enrichment: Multitiered Genomic Data Collection Across Evolutionary Scales, With Application to Chorus Frogs (Pseudacris).

Banker Sarah E SE Lemmon Alan R AR Hassinger Alyssa Bigelow AB Dye Mysia M Holland Sean D SD Kortyna Michelle L ML Ospina Oscar E OE Ralicki Hannah H Lemmon Emily Moriarty EM

Systematic biology 20200701 4

Determining the optimal targets of genomic subsampling for phylogenomics, phylogeography, and population genomics remains a challenge for evolutionary biologists. Of the available methods for subsampling the genome, hybrid enrichment (sequence capture) has become one of the primary means of data collection for systematics, due to the flexibility and cost efficiency of this approach. Despite the utility of this method, information is lacking as to what genomic targets are most appropriate for add ...[more]

PMID: 31886503

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Project description:BackgroundSpecies interactions can promote mating behavior divergence, particularly when these interactions are costly due to maladaptive hybridization. Selection against hybridization can indirectly cause evolution of reproductive isolation within species, a process termed cascade reinforcement. This process can drive incipient speciation by generating divergent selection pressures among populations that interact with different species assemblages. Theoretical and empirical studies indicate that divergent selection on gene expression networks has the potential to increase reproductive isolation among populations. After identifying candidate synaptic transmission genes derived from neurophysiological studies in anurans, we test for divergence of gene expression in a system undergoing cascade reinforcement, the Upland Chorus Frog (Pseudacris feriarum).ResultsOur analyses identified seven candidate synaptic transmission genes that have diverged between ancestral and reinforced populations of P. feriarum, including five that encode synaptic vesicle proteins. Our gene correlation network analyses revealed four genetic modules that have diverged between these populations, two possessing a significant concentration of neurotransmission enrichment terms: one for synaptic membrane components and the other for metabolism of the neurotransmitter nitric oxide. We also ascertained that a greater number of genes have diverged in expression by geography than by sex. Moreover, we found that more genes have diverged within females as compared to males between populations. Conversely, we observed no difference in the number of differentially-expressed genes within the ancestral compared to the reinforced population between the sexes.ConclusionsThis work is consistent with the idea that divergent selection on mating behaviors via cascade reinforcement contributed to evolution of gene expression in P. feriarum. Although our study design does not allow us to fully rule out the influence of environment and demography, the fact that more genes diverged in females than males points to a role for cascade reinforcement. Our discoveries of divergent candidate genes and gene networks related to neurotransmission support the idea that neural mechanisms of acoustic mating behaviors have diverged between populations, and agree with previous neurophysiological studies in frogs. Increasing support for this hypothesis, however, will require additional experiments under common garden conditions. Our work points to the importance of future replicated and tissue-specific studies to elucidate the relative contribution of gene expression divergence to the evolution of reproductive isolation during incipient speciation.

Project description:Reinforcement contact zones, which are secondary contact zones where species are diverging in reproductive behaviors due to selection against hybridization, represent natural laboratories for studying speciation-in-action. Here, we examined replicate localities across the entire reinforcement contact zone between North American chorus frogs Pseudacris feriarum and P. nigrita to investigate geographic variation in hybridization frequencies and to assess whether reinforcement may have contributed to increased genetic divergence within species. Previous work indicated these species have undergone reproductive character displacement (RCD) in male acoustic signals and female preferences due to reinforcement. We also examined acoustic signal variation across the contact zone to assess whether signal characteristics reliably predict hybrid index and to elucidate whether the degree of RCD predicts hybridization rate. Using microsatellites, mitochondrial sequences, and acoustic signal information from >1,000 individuals across >50 localities and ten sympatric focal regions, we demonstrate: (1) hybridization occurs and (2) varies substantially across the geographic range of the contact zone, (3) hybridization is asymmetric and in the direction predicted from observed patterns of asymmetric RCD, (4) in one species, genetic distance is higher between conspecific localities where one or both have been reinforced than between nonreinforced localities, after controlling for geographic distance, (5) acoustic signal characters strongly predict hybrid index, and (6) the degree of RCD does not strongly predict admixture levels. By showing that hybridization occurs in all sympatric localities, this study provides the fifth and final line of evidence that reproductive character displacement is due to reinforcement in the chorus frog contact zone. Furthermore, this work suggests that the dual action of cascade reinforcement and partial geographic isolation is promoting genetic diversification within one of the reinforced species.

Project description:The European water frog Pelophylax esculentus is a natural hybrid between P. lessonae (genotype LL) and P. ridibundus (RR). It reproduces through hybridogenesis, eliminating one parental genome from its germline and producing gametes containing the genome of the other parental species. According to previous studies, this elimination and transmission pattern is very diverse. In mixed populations, where only diploid hybrids (LR) live in sympatry and mate with one or both parental species, the excluded genome varies among regions, and the remaining genome is transmitted clonally to haploid gametes. In all-hybrid populations consisting of diploid (LR) and triploid (LLR and/or LRR) frogs, diploid individuals also produce gametes clonally (1n in males, 2n in females), whereas triploids eliminate the genome they have in single copy and produce haploid gametes containing the recombined other genome. However, here, too, regional differences seem to exist, and some triploids have been reported to produce diploid gametes. In order to systematically study such regional and genotype differences in gamete production, their potential origin, and their consequences for the breeding system, we sampled frogs from five populations in three European countries, performed crossing experiments, and investigated the genetic variation through microsatellite analysis. For four populations, one in Poland, two in Germany, and one in Slovakia, our results confirmed the elimination and transmission pattern described above. In one Slovakian population, however, we found a totally different pattern. Here, triploid males (LLR) produce sperm with a clonally transmitted diploid LL genome, rather than a haploid recombined L genome, and LR females clonally produce haploid R eggs, rather than diploid LR eggs. These differences among the populations in gamete production go along with differences in genomotype composition, breeding system (i.e., the way triploids are produced), and genetic variation. These differences are strong evidence for a polyphyletic origin of triploids. Moreover, our findings shed light on the evolutionary potential inherent to the P. esculentus complex, where rare events due to untypical gametogenetic processes can lead to the raise, the perpetuation, and the dispersion of new evolutionary significant lineages which may also deserve special conservation measures.

Dataset Information

Hierarchical Hybrid Enrichment: Multitiered Genomic Data Collection Across Evolutionary Scales, With Application to Chorus Frogs (Pseudacris).

Publications

Hierarchical Hybrid Enrichment: Multitiered Genomic Data Collection Across Evolutionary Scales, With Application to Chorus Frogs (Pseudacris).

Similar Datasets

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