Mitochondrial DNA under siege in avian phylogeography

Mitochondrial DNA (mtDNA) has been the workhorse of research in phylogeography for almost two decades. However, concerns with basing evolutionary interpretations on mtDNA results alone have been voiced since the inception of such studies. Recently, some authors have suggested that the potential problems with mtDNA are so great that inferences about population structure and species limits are unwarranted unless corroborated by other evidence, usually in the form of nuclear gene data. Here we review the relative merits of mitochondrial and nuclear phylogeographical studies, using birds as an exemplar class of organisms. A review of population demographic and genetic theory indicates that mitochondrial and nuclear phylogeographical results ought to concur for both geographically unstructured populations and for populations that have long histories of isolation. However, a relatively common occurrence will be shallow, but geographically structured mtDNA trees--without nuclear gene corroboration--for populations with relatively shorter periods of isolation. This is expected because of the longer coalescence times of nuclear genes (approximately four times that of mtDNA); such cases do not contradict the mtDNA inference of recent isolation and evolutionary divergence. Rather, the nuclear markers are more lagging indicators of changes in population structure. A review of the recent literature on birds reveals the existence of relatively few cases in which nuclear markers contradict mitochondrial markers in a fashion not consistent with coalescent theory. Preliminary information from nuclear genes suggests that mtDNA patterns will prove to be robust indicators of patterns of population history and species limits. At equilibrium, mitochondrial loci are generally a more sensitive indicator of population structure than are nuclear loci, and mitochondrial estimates of F(ST)-like statistics are generally expected to exceed nuclear ones. Hence, invoking behavioural or ecological explanations of such differences is not parsimonious. Nuclear genes will prove important for quantitative estimates of the depths of haplotype trees, rates of population growth and values of gene flow.     

Statistical phylogeography

While studies of phylogeography and speciation in the past have largely focused on the documentation or detection of significant patterns of population genetic structure, the emerging field of statistical phylogeography aims to infer the history and processes underlying that structure, and to provide objective, rather than ad hoc explanations. Methods for parameter estimation are now commonly used to make inferences about demographic past. Although these approaches are well developed statistically, they typically pay little attention to geographical history. In contrast, methods that seek to reconstruct phylogeographic history are able to consider many alternative geographical scenarios, but are primarily nonstatistical, making inferences about particular biological processes without explicit reference to stochastically derived expectations. We advocate the merging of these two traditions so that statistical phylogeographic methods can provide an accurate representation of the past, consider a diverse array of processes, and yet yield a statistical estimate of that history. We discuss various conceptual issues associated with statistical phylogeographic inferences, considering especially the stochasticity of population genetic processes and assessing the confidence of phylogeographic conclusions. To this end, we present some empirical examples that utilize a statistical phylogeographic approach, and then by contrasting results from a coalescent-based approach to those from Templeton's nested cladistic analysis (NCA), we illustrate the importance of assessing error. Because NCA does not assess error in its inferences about historical processes or contemporary gene flow, we performed a small-scale study using simulated data to examine how our conclusions might be affected by such unconsidered errors. NCA did not identify the processes used to simulate the data, confusing among deterministic processes and the stochastic sorting of gene lineages. There is as yet insufficient justification of NCA's ability to accurately infer or distinguish among alternative processes. We close with a discussion of some unresolved problems of current statistical phylogeographic methods to propose areas in need of future development.     

The Bassian Isthmus and the major ocean currents of southeast Australia influence the phylogeography and population structure of a southern Australian intertidal barnacle Catomerus polymerus (Darwin)

Southern Australia is currently divided into three marine biogeographical provinces based on faunal distributions and physical parameters. These regions indicate eastern and western distributions, with an overlap occurring in the Bass Strait in Victoria. However, studies indicate that the boundaries of these provinces vary depending on the species being examined, and in particular on the mode of development employed by that species, be they direct developers or planktonic larvae dispersers. Mitochondrial DNA sequence analysis of the surf barnacle Catomerus polymerus in southern Australia revealed an east-west phylogeographical split involving two highly divergent clades (cytochrome oxidase I 3.5 +/- 0.76%, control region 6.7 +/- 0.65%), with almost no geographical overlap. Spatial genetic structure was not detected within either clade, indicative of a relatively long-lived planktonic larval phase. Five microsatellite loci indicated that C. polymerus populations exhibit relatively high levels of genetic divergence, and fall into four subregions: eastern Australia, central Victoria, western Victoria and Tasmania, and South Australia. F(ST) values between eastern Australia (from the eastern mitochondrial DNA clade) and the remaining three subregions ranged from 0.038 to 0.159, with other analyses indicating isolation by distance between the subregions of western mitochondrial origin. We suggest that the east-west division is indicative of allopatric divergence resulting from the emergence of the Bassian land-bridge during glacial maxima, preventing gene flow between these two lineages. Subsequently, contemporary ecological conditions, namely the East Australian, Leeuwin, and Zeehan currents and the geographical disjunctions at the Coorong and Ninety Mile Beach are most likely responsible for the four subregions indicated by the microsatellite data.     

First DNA sequences from Asian cave bear fossils reveal deep divergences and complex phylogeographic patterns

Until recently, cave bears were believed to have only inhabited Europe. However, recent morphological evidence suggests that cave bears' geographic range extended as far east as Transbaikalia, Eastern Siberia. These Asian cave bears were morphologically distinct from European cave bears. However, how they related to European lineages remains unclear, stressing the need to assess the phylogenetic and phylogeographic relationship between Asian cave bears and their European relatives. In this work, we address this issue using a 227 base-pair fragment of the mitochondrial control region obtained from nine fossil bone samples from eight sites from the Urals, Caucasus, Altai Mountains, Ukraine and Yana River region in Eastern Siberia. Results of the phylogenetic analyses indicate that (i) the cave bear from the Yana River is most closely related to cave bears from the Caucasus region; (ii) the Caucasus/Yana group of bears is genetically very distinct from both European cave bears and brown bears, suggesting that these bears could represent an independent species; and (iii) the Western European cave bear lineage reached at least temporarily to the Altai Mountains, 7000 km east of their known centre of distribution. These results suggest that the diversity of cave bears was greater than previously believed, and that they could survive in a much wider range of ecological conditions than previously assumed. They also agree with recent studies on other extinct and extant species, such as wolves, hyenas and steppe bison, which have also revealed higher genetic and ecological diversity in Pleistocene populations than previously known.     

Parapatric divergence of sympatric morphs in a salamander: incipient speciation on Long Island?

Speciation is often categorized based on geographic modes (allopatric, parapatric or sympatric). Although it is widely accepted that species can arise in allopatry and then later become sympatrically or parapatrically distributed, patterns in the opposite direction are also theoretically possible (e.g. sympatric lineages or ecotypes becoming parapatric), but such patterns have not been shown at a macrogeographic scale. Here, we analyse genetic, climatic, ecological and morphological data and show that two typically sympatric colour morphs of the salamander Plethodon cinereus (redback and leadback) appear to have become parapatrically distributed on Long Island, New York, with pure‐redback populations in the west and pure‐leadback populations in the east (and polymorphic populations in between and on the mainland). In addition, the pure‐leadback populations in eastern Long Island are genetically, ecologically and morphologically divergent from both mainland and other Long Island populations, suggesting the possibility of incipient speciation. This parapatric separation seems to be related to the different ecological preferences of the two morphs, preferences which are present on the mainland and across Long Island. These results potentially support the idea that spatial segregation of sympatric ecotypes may sometimes play an important part in parapatric speciation.