Ryan C. Garrick

Landscape modelling of gene flow: improved power using conditional genetic distance derived from the topology of population networks

Landscape genetics is a burgeoning field of interest that focuses on how site‐specific factors influence the distribution of genetic variation and the genetic connectivity of individuals and populations. In this manuscript, we focus on two methodological extensions for landscape genetic analyses: the use of conditional genetic distance (cGD) derived from population networks and the utility of extracting potentially confounding effects caused by correlations between phylogeographic history and contemporary ecological factors. Individual‐based simulations show that when describing the spatial distribution of genetic variation, cGD consistently outperforms the traditional genetic distance measure of linearized FST under both 1‐ and 2‐dimensional stepping stone models and Cavalli‐Sforza and Edward’s chord distance Dc in 1‐dimensional landscapes. To show how to identify and extract the effects of phylogeographic history prior to embarking on landscape genetic analyses, we use nuclear genotypic data from the Sonoran desert succulent Euphorbia lomelii (Euphrobiaceae), for which a detailed phylogeographic history has previously been determined. For E. lomelii, removing the effect of phylogeographic history significantly influences our ability to infer both the identity and the relative importance of spatial and bio‐climatic variables in subsequent landscape genetic analyses. We close by discussing the utility of cGD in landscape genetic analyses.

Fine-Scale Phylogeographic Congruence Despite Demographic Incongruence in Two Low-Mobility Saproxylic Springtails

Abstract Evolutionary trajectories of codistributed taxa with comparable ecological preferences and dispersal abilities may be similarly impacted by historical landscape-level processes. Species’ responses to changes in a shared biogeographic landscape may be purely concerted, completely independent, or classified as falling within an intermediate part of the continuum bounded by these two extremes. With sufficient molecular data, temporal contrasts of congruence among taxa with respect to these responses can be made. Such contrasts provide insights into the relative influence of ancient versus more recent climatic (and other) impacts on genetic structuring. Using phylogenetic, allele frequency, and genotypic data from two low-mobility, rotting-log-adapted (saproxylic) springtail species (Collembola) from an isolated 100-km-long section of the Great Dividing Range in southeastern Australia, we tested the concerted-response hypothesis over three timescales. Tests of phylogeographic, demographic, and contemporary population-genetic congruence were performed using an integrative approach that draws on both direct (pattern-based) and indirect (scenario-based) analyses. Our data revealed a general pattern of broad-scale similarities in species’ responses to the interaction between Pleistocene climatic cycles and landscape setting, overlaid with some species-specific differences on local geographic and more recent temporal scales. This general pattern of phylogeographic congruence was accompanied by evidence for contemporaneous demographic incongruence indicating that, even at relatively small spatial scales, biogeographic context can exert an overarching influence on genetic structuring.

Nuclear gene phylogeography using PHASE: dealing with unresolved genotypes, lost alleles, and systematic bias in parameter estimation

BackgroundA widely-used approach for screening nuclear DNA markers is to obtain sequence data and use bioinformatic algorithms to estimate which two alleles are present in heterozygous individuals. It is common practice to omit unresolved genotypes from downstream analyses, but the implications of this have not been investigated. We evaluated the haplotype reconstruction method implemented by PHASE in the context of phylogeographic applications. Empirical sequence datasets from five non-coding nuclear loci with gametic phase ascribed by molecular approaches were coupled with simulated datasets to investigate three key issues: (1) haplotype reconstruction error rates and the nature of inference errors, (2) dataset features and genotypic configurations that drive haplotype reconstruction uncertainty, and (3) impacts of omitting unresolved genotypes on levels of observed phylogenetic diversity and the accuracy of downstream phylogeographic analyses.ResultsWe found that PHASE usually had very low false-positives (i.e., a low rate of confidently inferring haplotype pairs that were incorrect). The majority of genotypes that could not be resolved with high confidence included an allele occurring only once in a dataset, and genotypic configurations involving two low-frequency alleles were disproportionately represented in the pool of unresolved genotypes. The standard practice of omitting unresolved genotypes from downstream analyses can lead to considerable reductions in overall phylogenetic diversity that is skewed towards the loss of alleles with larger-than-average pairwise sequence divergences, and in turn, this causes systematic bias in estimates of important population genetic parameters.ConclusionsA combination of experimental and computational approaches for resolving phase of segregating sites in phylogeographic applications is essential. We outline practical approaches to mitigating potential impacts of computational haplotype reconstruction on phylogeographic inferences. With targeted application of laboratory procedures that enable unambiguous phase determination via physical isolation of alleles from diploid PCR products, relatively little investment of time and effort is needed to overcome the observed biases.

Phylogeography recapitulates topography: very fine‐scale local endemism of a saproxylic ‘giant’ springtail at Tallaganda in the Great Dividing Range of south–east Australia

Comparative phylogeography can reveal processes and historical events that shape the biodiversity of species and communities. As part of a comparative research program, the phylogeography of a new, endemic Australian genus and species of log‐dependent (saproxylic) collembola was investigated using mitochondrial sequences, allozymes and anonymous single‐copy nuclear markers. We found the genetic structure of the species corresponds with five a priori microbiogeographical regions, with population subdivision at various depths owing to palaeoclimatic influences. Closely related mtDNA haplotypes are codistributed within a single region or occur in adjacent regions, nuclear allele frequencies are more similar among more proximate populations, and interpopulation migration is rare. Based on mtDNA divergence, a late Miocene–late Pliocene coalescence is likely. The present‐day distribution of genetic diversity seems to have been impacted by three major climatic events: Pliocene cooling and drying (2.5–7 million years before present, Mybp), early Pleistocene wet‐dry oscillations (c. 1.2 Mybp) and the more recent glacial‐interglacial cycles that have characterized the latter part of the Quaternary (< 0.4 Mybp).

A tale of two flatties : different responses of two terrestrial flatworms to past environmental climatic fluctuations at Tallaganda in montane southeastern Australia.

Comparative phylogeographic studies of animals with low mobility and/or high habitat specificity remain rare, yet such organisms may hold fine‐grained palaeoecological signal. Comparisons of multiple, codistributed species can elucidate major historical events. As part of a multitaxon programme, mitochondrial cytochrome oxidase I (COI) variation was analysed in two species of terrestrial flatworm, Artioposthia lucasi and Caenoplana coerulea. We applied coalescent demographic estimators and nested clade analysis to examine responses to past, landscape‐scale, cooling‐drying events in a model system of montane forest (Tallaganda). Correspondence of haplotype groups in both species to previously proposed microbiogeographic regions indicates at least four refuges from cool, dry conditions. The region predicted to hold the highest quality refuges (the Eastern Slopes Region), is indicated to have been a long‐term refuge in both species, but so are several other regions. Coalescent analyses suggest that populations of A. lucasi are declining, while C. coerulea is expanding, although stronger population substructure in the former could yield similar patterns in the data. The differences in spatial and temporal genetic variation in the two species could be explained by differences in ecological attributes: A. lucasi is predicted to have lower dispersal ability but may be better able to withstand cold conditions. Thus, different contemporary population dynamics may reflect different responses to recent (Holocene) climate warming. The two species show highly congruent patterns of catchment‐based local genetic endemism with one another and with previously studied slime‐mould grazing Collembola.

Catchments catch all: long-term population history of a giant springtail from the southeast Australian highlands — a multigene approach

Phylogeography can reveal evolutionary processes driving natural genetic‐geographical patterns in biota, providing an empirical framework for optimizing conservation strategies. The long‐term population history of a rotting‐log‐adapted giant springtail (Collembola) from montane southeast Australia was inferred via joint analysis of mitochondrial and multiple nuclear gene genealogies. Contemporary populations were identified using multilocus nuclear genotype clustering. Very fine‐scale sampling combined with nested clade and coalescent‐based analyses of sequences from mitochondrial cytochrome oxidase I and three unlinked nuclear loci uncovered marked population structure, deep molecular divergences, and abrupt phylogeographical breaks over distances on the order of tens of kilometres or less. Despite adaptations that confer low mobility, rare long‐distance gene flow was implicated: novel computer simulations that jointly modelled stochasticity inherent in coalescent processes and that of DNA sequence evolution showed that incomplete lineage sorting alone was unable to explain the observed spatial‐genetic patterns. Impacts of Pleistocene or earlier climatic cycles were detected on multiple timescales, and at least three putative moist forest refuges were identified. Water catchment divisions predict phylogeographical patterning and present‐day population structure with high precision, and may serve as an excellent surrogate for biodiversity indication in sedentary arthropods from topographically heterogeneous montane temperate forests.

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.

Inference of Population History by Coupling Exploratory and Model-Driven Phylogeographic Analyses

Understanding the nature, timing and geographic context of historical events and population processes that shaped the spatial distribution of genetic diversity is critical for addressing questions relating to speciation, selection, and applied conservation management. Cladistic analysis of gene trees has been central to phylogeography, but when coupled with approaches that make use of different components of the information carried by DNA sequences and their frequencies, the strength and resolution of these inferences can be improved. However, assessing concordance of inferences drawn using different analytical methods or genetic datasets, and integrating their outcomes, can be challenging. Here we overview the strengths and limitations of different types of genetic data, analysis methods, and approaches to historical inference. We then turn our attention to the potentially synergistic interactions among widely-used and emerging phylogeographic analyses, and discuss some of the ways that spatial and temporal concordance among inferences can be assessed. We close this review with a brief summary and outlook on future research directions.

Montane refuges and topographic complexity generate and maintain invertebrate biodiversity: recurring themes across space and time

If a common set of landscape characteristics seem to predict spatial patterns of biodiversity in several regions with different biogeographic histories and community compositions, these could inform conservation. Two papers recently published in Journal of Insect Conservation provided evidence that topographic heterogeneity can play a major role in harbouring invertebrate community biodiversity, and that upland areas potentially function as refugia from infrequent but severe climatic conditions that occur over ecological timescales. Similar findings are being echoed in the growing body of phylogeographic literature on terrestrial invertebrates from montane landscape settings. The purpose of this short communication is to place the two recently published papers into a broader context. Phylogeographic studies usually focus on genetic diversity within and among populations, and at relatively deep evolutionary timescales. The parallels that appear to be emerging across different levels of biological organisation and temporal spectra suggest that (1) microevolutionary processes operating at the level of populations may ‘scale-up’ to macroevolutionary processes operating at the level of species or higher, and (2) certain landscape features—particularly topography—may be particularly important when formulating strategies to protect terrestrial invertebrate biodiversity.

Lineage fusion in Galápagos giant tortoises.

Although many classic radiations on islands are thought to be the result of repeated lineage splitting, the role of past fusion is rarely known because during these events, purebreds are rapidly replaced by a swarm of admixed individuals. Here, we capture lineage fusion in action in a Galápagos giant tortoise species, Chelonoidis becki, from Wolf Volcano (Isabela Island). The long generation time of Galápagos tortoises and dense sampling (841 individuals) of genetic and demographic data were integral in detecting and characterizing this phenomenon. In C. becki, we identified two genetically distinct, morphologically cryptic lineages. Historical reconstructions show that they colonized Wolf Volcano from Santiago Island in two temporally separated events, the first estimated to have occurred ~199 000 years ago. Following arrival of the second wave of colonists, both lineages coexisted for approximately ~53 000 years. Within that time, they began fusing back together, as microsatellite data reveal widespread introgressive hybridization. Interestingly, greater mate selectivity seems to be exhibited by purebred females of one of the lineages. Forward‐in‐time simulations predict rapid extinction of the early arriving lineage. This study provides a rare example of reticulate evolution in action and underscores the power of population genetics for understanding the past, present and future consequences of evolutionary phenomena associated with lineage fusion.