Ariadna E. Morales

The evolution of phylogeographic data sets.

Empirical phylogeographic studies have progressively sampled greater numbers of loci over time, in part motivated by theoretical papers showing that estimates of key demographic parameters improve as the number of loci increases. Recently, next‐generation sequencing has been applied to questions about organismal history, with the promise of revolutionizing the field. However, no systematic assessment of how phylogeographic data sets have changed over time with respect to overall size and information content has been performed. Here, we quantify the changing nature of these genetic data sets over the past 20 years, focusing on papers published in Molecular Ecology. We found that the number of independent loci, the total number of alleles sampled and the total number of single nucleotide polymorphisms (SNPs) per data set has improved over time, with particularly dramatic increases within the past 5 years. Interestingly, uniparentally inherited organellar markers (e.g. animal mitochondrial and plant chloroplast DNA) continue to represent an important component of phylogeographic data. Single‐species studies (cf. comparative studies) that focus on vertebrates (particularly fish and to some extent, birds) represent the gold standard of phylogeographic data collection. Based on the current trajectory seen in our survey data, forecast modelling indicates that the median number of SNPs per data set for studies published by the end of the year 2016 may approach ~20 000. This survey provides baseline information for understanding the evolution of phylogeographic data sets and underscores the fact that development of analytical methods for handling very large genetic data sets will be critical for facilitating growth of the field.

PHRAPL: Phylogeographic Inference Using Approximate Likelihoods

Abstract.— The demographic history of most species is complex, with multiple evolutionary processes combining to shape the observed patterns of genetic diversity. To infer this history, the discipline of phylogeography has (to date) used models that simplify the historical demography of the focal organism, for example by assuming or ignoring ongoing gene flow between populations or by requiring a priori specification of divergence history. Since no single model incorporates every possible evolutionary process, researchers rely on intuition to choose the models that they use to analyze their data. Here, we describe an approximate likelihood approach that reduces this reliance on intuition. PHRAPL allows users to calculate the probability of a large number of complex demographic histories given a set of gene trees, enabling them to identify the most likely underlying model and estimate parameters for a given system. Available model parameters include coalescence time among populations or species, gene flow, and population size. We describe the method and test its performance in model selection and parameter estimation using simulated data. We also compare model probabilities estimated using our approximate likelihood method to those obtained using standard analytical likelihood. The method performs well under a wide range of scenarios, although this is sometimes contingent on sampling many loci. In most scenarios, as long as there are enough loci and if divergence among populations is sufficiently deep, PHRAPL can return the true model in nearly all simulated replicates. Parameter estimates from the method are also generally accurate in most cases. PHRAPL is a valuable new method for phylogeographic model selection and will be particularly useful as a tool to more extensively explore demographic model space than is typically done or to estimate parameters for complex models that are not readily implemented using current methods. Estimating relevant parameters using the most appropriate demographic model can help to sharpen our understanding of the evolutionary processes giving rise to phylogeographic patterns. [AIC; grid search; isolation‐with‐migration; migration rate; multispecies coalescent; parameter optimization; population genetics; tree topologies.]

Speciation with Gene Flow in North American Myotis Bats

Abstract Growing evidence supports the idea that species can diverge in the presence of gene flow. However, most methods of phylogeny estimation do not consider this process, despite the fact that ignoring gene flow is known to bias phylogenetic inference. Furthermore, studies that do consider divergence‐with‐gene‐flow typically do so by estimating rates of gene flow using a isolation‐with‐migration model (IM), rather than evaluating scenarios of gene flow (such as divergence‐with‐gene flow or secondary contact) that represent very different types of diversification. In this investigation, we aim to infer the recent phylogenetic history of a clade of western long‐eared bats while evaluating a number of different models that parameterize gene flow in a variety of ways. We utilize PHRAPL, a new tool for phylogeographic model selection, to compare the fit of a broad set of demographic models that include divergence, migration, or both among Myotis evotis, M. thysanodes and M. keenii. A genomic data set consisting of 808 loci of ultraconserved elements was used to explore such models in three steps using an incremental design where each successive set was informed by, and thus more focused than, the previous set of models. Specifically, the three steps were to (i) assess whether gene flow should be modeled and identify the best topologies, (ii) infer directionality of migration using the best topologies, and (iii) estimate the timing of gene flow. The best model (AIC model weight ∼0.98) included two divergence events ((M. evotis, M. thysanodes), M. keenii) accompanied by gene flow at the initial stages of divergence. These results provide a striking example of speciation‐with‐gene‐flow in an evolutionary lineage.

Evidence that Myotis lucifugus “Subspecies” are Five Nonsister Species, Despite Gene Flow

Abstract.— While genetic exchange between nonsister species was traditionally considered to be rare in mammals, analyses of molecular data in multiple systems suggest that it may be common. Interspecific gene flow, if present, is problematic for phylogenetic inference, particularly for analyses near the species level. Here, we explore how to detect and account for gene flow during phylogeny estimation using data from a clade of North American Myotis bats where previous results have led researchers to suspect that gene flow among lineages is present. Initial estimates of phylogenetic networks and species trees indicate that subspecies described within Myotis lucifugus are paraphyletic. In order to explore the extent to which gene flow is likely to interfere with phylogeny estimation, we use posterior predictive simulation and a novel Approximate Bayesian Computation approach based on gene tree distances. The former indicates that the species tree model is a poor fit to the data, and the latter provides evidence that a species tree with gene flow is a better fit. Taken together, we present evidence that the currently recognized M. lucifugus subspecies are paraphyletic, exchange alleles with other Myotis species in regions of secondary contact, and should be considered independent evolutionary lineages despite their morphological similarity.

Objective choice of phylogeographic models

Phylogeography seeks to discover the evolutionary processes that have given rise to organismal and genetic diversity. This requires explicit hypotheses (i.e., models) to be evaluated with genetic data in order to identify those hypotheses that best explain the data. In recent years, advancements in the model-based tools used to estimate phylogeographic parameters of interest such as gene flow, divergence time, and relationships among groups have been made. However, given the complexity of these models, available methods can typically only compare a handful of possible hypotheses, requiring researchers to specify in advance the small set of models to consider. Without formal quantitative approaches to model selection, researchers must rely on their intuition to formulate the model space to be explored. We explore the adequacy of intuitive choices made by researchers during the process of data analysis by reanalyzing 20 empirical phylogeographic datasets using PHRAPL, an objective tool for phylogeographic model selection. We show that the best models for most datasets include both gene flow and population divergence parameters, and that species tree methods (which do not consider gene flow) tend to be overly simplistic for many phylogeographic systems. Objective approaches to phylogeographic model selection offer an important complement to researcher intuition.

Genome-specific histories of divergence and introgression between an allopolyploid unisexual salamander lineage and two sexual species

Quantifying genetic introgression between sexual species and polyploid lineages traditionally thought to be asexual is an important step in understanding what factors drive the longevity of putatively asexual groups. However, the presence of multiple distinct subgenomes within a single lineage provides a significant logistical challenge to evaluating the origin of genetic variation in most polyploids. Here, we capitalize on three recent innovations—variation generated from ultraconserved elements (UCEs), bioinformatic techniques for assessing variation in polyploids, and model-based methods for evaluating historical gene flow—to measure the extent and tempo of introgression over the evolutionary history of an allopolyploid lineage of all-female salamanders and two ancestral sexual species. We first analyzed variation from more than a thousand UCEs using a reference mapping method developed for polyploids to infer subgenome specific patterns of variation in the all-female lineage. We then used PHRAPL to choose between sets of historical models that reflected different patterns of introgression and divergence between the genomes of the parental species and the same genomes found within the polyploids. Our analyses support a scenario in which the genomes sampled in unisexuals salamanders were present in the lineage ∼3.4 million years ago, followed by an extended period of divergence from their parental species. Recent secondary introgression has occurred at different times between each sexual species and their representative genomes within the unisexuals during the last 500,000 years. Sustained introgression of sexual genomes into the unisexual lineage has been the defining characteristic of their reproductive mode, but this study provides the first evidence that unisexual genomes have also undergone long periods of divergence without introgression. Unlike other unisexual, sperm-dependent taxa in which introgression is rare, the alternating periods of divergence and introgression between unisexual salamanders and their sexual relatives could reveal the scenarios in which the influx of novel genomic material is favored and potentially explain why these salamanders are among the oldest described unisexual animals.

Genome-specific histories of divergence and introgression between an allopolyploid unisexual salamander lineage and two ancestral sexual species: UNISEXUAL SALAMANDER INTROGRESSION

Quantifying introgression between sexual species and polyploid lineages traditionally thought to be asexual is an important step in understanding what drives the longevity of putatively asexual groups. Here, we capitalize on three recent innovations—ultraconserved element (UCE) sequencing, bioinformatic techniques for identifying genome‐specific variation in polyploids, and model‐based methods for evaluating historical gene flow—to measure the extent and tempo of introgression over the evolutionary history of an allopolyploid lineage of all‐female salamanders and two ancestral sexual species. Our analyses support a scenario in which the genomes sampled in unisexual salamanders last shared a common ancestor with genomes in their parental species ∼3.4 million years ago, followed by a period of divergence between homologous genomes. Recently, secondary introgression has occurred at different times with each sexual species during the last 500,000 years. Sustained introgression of sexual genomes into the unisexual lineage is the defining characteristic of their reproductive mode, but this study provides the first evidence that unisexual genomes have undergone long periods of divergence without introgression. Unlike other sperm‐dependent taxa in which introgression is rare, the alternating periods of divergence and introgression between unisexual salamanders and their sexual relatives could explain why these salamanders are among the oldest described unisexual animals.