Part II
COMPARATIVE PHYLOGEOGRAPHY IN A GENOMIC SENSE
Throughout the early phylogeographic era, cytoplasmic genomes (mitochondrial DNA in animals and chloroplast DNA in plants) provided the bulk of empirical genetic information for phylogeographic reconstructions. However, a long-appreciated fact is that these cytoplasmic genomes represent only a minuscule fraction of a species’ total hereditary pedigree, the vast majority of which is ensconced in nuclear DNA. Early attempts to extract useful phylogeographic information from the nuclear genome met mostly with failure, due to technical difficulties coupled with sex-based genetic recombination. In recent years, this situation has changed (to an arguable degree) due to the ongoing technological revolutions in next-generation sequencing and “big-data” genomics. How might phylogeographic inferences be impacted as new technologies extract more and more genetic information from loci in the recombining nuclear genome?
Each species has its own true phylogeographic past (extended intraspecific pedigree) through which its various loci have been transmitted and which therefore constitute a plethora of gene genealogies. For any species, genealogy and historical population demography are like opposite sides of the same coin: intimately connected. Coalescent theory offers a robust conceptual framework for translating the empirical phylogeographic structure of a “gene tree” (such as that provided by mtDNA) into inferences about a population’s demography history. Although the population pedigree of any species in effect contains (or consists of) multitudinous quasi-independent nuclear gene trees, the actual degree to which
a given pedigree constrains the topologies of multiple unlinked loci has received rather scant attention. In Chapter 5, John Wakeley and colleagues address this issue using population genetic models and computer simulations. By focusing attention on extreme demographic events (the occurrence of very large families in a pedigree, and on strong selective sweeps in the population’s recent past), the authors conclude that “only rather extreme versions of such events can be expected to structure population pedigrees in such a way that unlinked loci will show deviations from the standard predictions of population genetics, which average over population pedigrees.”
Rohan Mehta and colleagues (Chapter 6) continue this general theme of the fundamental distinction between gene trees and population (or species) trees, by addressing the probability of monophyly of a gene lineage on a species tree. Although such models (based on neutral coalescent theory) have long been employed to calculate the probability that a set of gene lineages is reciprocally monophyletic under the simplest case of a pair of sister taxa, the current authors extend such analyses to probabilities of gene-tree monophyly for genetic studies that span arbitrary numbers of multiple isolated populations or species.
One of several new types of nuclear data stemming from next-generation sequencing involves the recovery of SNPs (single nucleotide polymorphisms) from many thousands of unlinked nuclear genomic regions, even in nonmodel species. SNPs are increasingly being used to supplement more traditional phylogeographic datasets based on cytoplasmic genomic sequences or allelic profiles at relatively small numbers of microsatellite loci. In Chapter 7, Maria Thomé and Bryan Carstens employ a case-history approach (involving Brazilian frogs) to illustrate how such molecular information can be used to estimate historical population demographic parameters (such as population size and gene flow) under a wide variety of evolutionary models. Their take-home message is that an objective approach to phylogeographic inference should entail calculating the probability of multiple demographic models given the data and then subsequently ranking these models using information theory. The chapter’s framework also allows the authors to express their own views on the ever-changing epistemology of phylogeographic inference.
Anna Papadopoulou and Lacey Knowles (Chapter 8) expand on the topic of phylogeographic models by tracing and critiquing the historical emphasis on genealogical concordance in comparative phylogeography. Such concordance generally refers to shared phylogeographic patterns, either across multiple loci within extant species or across particular genes of multiple codistributed species. The authors question whether concordance in general is a uniformly useful criterion for evaluating alternative phylogeographic hypotheses, by emphasizing taxon-specific traits that
may predict concordance or discordance among datasets and species. The authors bolster their reservations with case studies illustrating the many possible ways that genealogical discordance (the antithesis of concordance) can arise in particular situations.
Scott Edwards and colleagues (Chapter 9) conclude this section of the book by providing an overview of the impact of cutting-edge molecular technologies (such as various expressions of next-generation sequencing) on the trajectory of the fields of phylogeography and phylogenetics in the genomics era. As empirically illustrated by the authors’ comparative genetic research spanning diverse vertebrate taxa across northern Australia, the emerging discipline of phylogenomics will call for a greater appreciation of reticulation during the evolutionary process, both within genomes in the form of genetic recombination, and across populations and species in the forms of gene flow and introgression. In this important sense, the arenas of comparative phylogeography and interspecific phylogenetics can again be seen as lying along a conceptual continuum of historical evolutionary genetic phenomena, from population-level separations to deeper organismal divergences.
