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1.
bioRxiv ; 2023 Oct 21.
Article in English | MEDLINE | ID: mdl-37905020

ABSTRACT

Despite newly formed polyploids being subjected to myriad fitness consequences, the relative prevalence of polyploidy both contemporarily and in ancestral branches of the tree of life suggests alternative advantages that outweigh these consequences. One proposed advantage is that polyploids have an elevated adaptive potential that enables them to colonize novel habitats such as previously glaciated areas. However, previous research conducted in diploids suggests that range expansion comes with a fitness cost as deleterious mutations may fix rapidly on the expansion front. Here, we interrogate the potential consequences of expansion in polyploids by conducting spatially explicit forward-in-time simulations of autopolyploids, allopolyploids, and diploids to investigate how ploidy and inheritance patterns impact the relative ability of polyploids to expand their range. We show that under realistic dominance models, autopolyploids suffer greater fitness reductions than diploids as a result of range expansion due to the fixation of increased mutational load that is masked in the range core. Alternatively, the disomic inheritance of allopolyploids provides a shield to this fixation resulting in minimal fitness consequences under an empirically estimated DFE. In light of this advantage provided by disomy, we investigate how range expansion may influence cytogenetic diploidization through the reversion to disomy in autotetraploids. We show that under both a model of where the mode of inheritance is determined by a small number of loci and a model where inheritance is regulated by chromosomal similarity, disomy evolves more rapidly on the expansion front than in the range core, and that this dynamic inheritance model has additional effects on fitness. Together our results point to a complex interaction between dominance, ploidy, inheritance, and recombination on fitness as a population spreads across a geographic range.

2.
Mol Ecol ; 32(17): 4863-4879, 2023 09.
Article in English | MEDLINE | ID: mdl-37401503

ABSTRACT

After polyploid species are formed, interactions between diploid and polyploid lineages may generate additional diversity in novel cytotypes and phenotypes. In anurans, mate choice by acoustic communication is the primary method by which individuals identify their own species and assess suitable mates. As such, the evolution of acoustic signals is an important mechanism for contributing to reproductive isolation and diversification in this group. Here, we estimate the biogeographical history of the North American grey treefrog complex, consisting of the diploid Hyla chrysoscelis and the tetraploid Hyla versicolor, focusing specifically on the geographical origin of whole genome duplication and the expansion of lineages out of glacial refugia. We then test for lineage-specific differences in mating signals by applying comparative methods to a large acoustic data set collected over 52 years that includes >1500 individual frogs. Along with describing the overall biogeographical history and call diversity, we found evidence that the geographical origin of H. versicolor and the formation of the midwestern polyploid lineage are both associated with glacial limits, and that the southwestern polyploid lineage is associated with a shift in acoustic phenotype relative to the diploid lineage with which they share a mitochondrial lineage. In H. chrysoscelis, we see that acoustic signals are largely split by Eastern and Western lineages, but that northward expansion along either side of the Appalachian Mountains is associated with further acoustic diversification. Overall, results of this study provide substantial clarity on the evolution of grey treefrogs as it relates to their biogeography and acoustic communication.


Subject(s)
Anura , Polyploidy , Animals , Anura/genetics , Diploidy , North America , Appalachian Region
3.
Genetics ; 224(2)2023 05 26.
Article in English | MEDLINE | ID: mdl-37067864

ABSTRACT

Numerous studies over the last decade have demonstrated the utility of machine learning methods when applied to population genetic tasks. More recent studies show the potential of deep-learning methods in particular, which allow researchers to approach problems without making prior assumptions about how the data should be summarized or manipulated, instead learning their own internal representation of the data in an attempt to maximize inferential accuracy. One type of deep neural network, called Generative Adversarial Networks (GANs), can even be used to generate new data, and this approach has been used to create individual artificial human genomes free from privacy concerns. In this study, we further explore the application of GANs in population genetics by designing and training a network to learn the statistical distribution of population genetic alignments (i.e. data sets consisting of sequences from an entire population sample) under several diverse evolutionary histories-the first GAN capable of performing this task. After testing multiple different neural network architectures, we report the results of a fully differentiable Deep-Convolutional Wasserstein GAN with gradient penalty that is capable of generating artificial examples of population genetic alignments that successfully mimic key aspects of the training data, including the site-frequency spectrum, differentiation between populations, and patterns of linkage disequilibrium. We demonstrate consistent training success across various evolutionary models, including models of panmictic and subdivided populations, populations at equilibrium and experiencing changes in size, and populations experiencing either no selection or positive selection of various strengths, all without the need for extensive hyperparameter tuning. Overall, our findings highlight the ability of GANs to learn and mimic population genetic data and suggest future areas where this work can be applied in population genetics research that we discuss herein.


Subject(s)
Biological Evolution , Genome, Human , Humans , Linkage Disequilibrium , Machine Learning , Privacy
4.
Mol Biol Evol ; 39(2)2022 02 03.
Article in English | MEDLINE | ID: mdl-34791374

ABSTRACT

Polyploid speciation has played an important role in evolutionary history across the tree of life, yet there remain large gaps in our understanding of how polyploid species form and persist. Although systematic studies have been conducted in numerous polyploid complexes, recent advances in sequencing technology have demonstrated that conclusions from data-limited studies may be spurious and misleading. The North American gray treefrog complex, consisting of the diploid Hyla chrysoscelis and the tetraploid H. versicolor, has long been used as a model system in a variety of biological fields, yet all taxonomic studies to date were conducted with only a few loci from nuclear and mitochondrial genomes. Here, we utilized anchored hybrid enrichment and high-throughput sequencing to capture hundreds of loci along with whole mitochondrial genomes to investigate the evolutionary history of this complex. We used several phylogenetic and population genetic methods, including coalescent simulations and testing of polyploid speciation models with approximate Bayesian computation, to determine that H. versicolor was most likely formed via autopolyploidization from a now extinct lineage of H. chrysoscelis. We also uncovered evidence of significant hybridization between diploids and tetraploids where they co-occur, and show that historical hybridization between these groups led to the re-formation of distinct polyploid lineages following the initial whole-genome duplication event. Our study indicates that a wide variety of methods and explicit model testing of polyploid histories can greatly facilitate efforts to uncover the evolutionary history of polyploid complexes.


Subject(s)
Gene Duplication , Polyploidy , Animals , Anura/genetics , Bayes Theorem , North America , Phylogeny
5.
Syst Biol, v. 20, n. 1, p. 1-25, jan. 2022
Article in English | Sec. Est. Saúde SP, SESSP-IBPROD, Sec. Est. Saúde SP | ID: bud-4119

ABSTRACT

Brazilian continental islands represent a natural laboratory to study speciation driven by recent phenotypic and genotypic divergence. The Bothrops jararaca species group is distributed in the Brazilian Atlantic Forest and on most of the Brazilian continental islands. The group is currently composed of the mainland common lancehead (B. jararaca) and four insular species (B. alcatraz, B. insularis, B. otavioi, and B. sazimai). Here, we evaluate mitochondrial DNA and morphological diversity of the B. jararaca species group and aim to provide additional evidence to understand insularization processes on the Brazilian coast. Our results, interpreted together with a comprehensive review of geomorphological data, provide a new conceptual framework for understanding the colonization process of the Brazilian continental islands. This framework suggests a history of multiple rounds of periodic isolation and reconnection between insular populations and their mainland relatives throughout the last 420,000 years. Furthermore, although some insular populations may have speciated prior to the last glacial maximum, other species likely diverged within the last 11,000 years. Additionally, the repeated evolution of size and dietary shift in the B. jararaca species group suggests a remarkable case of convergent adaptation. Our study provides evidence that the Bothrops from Ilha da Moela (Brazilian state of São Paulo) represents an undescribed species, presenting a distinct phenotype, and an exclusive history of isolation and adaptation. We describe this unique lancehead as a new species and we suggest it should be listed as critically endangered based on its endemicity to a small island that is severely impacted by constant and longstanding human presence.

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