The history and purview of phylogeography: a personal reflection

Last year marked the 10th anniversary of the birth of phylogeography as a formal discipline. However, the field's gestation began in the mid-1970s with the introduction of mitochondrial (mt) DNA analyses to population genetics, and to the profound shift toward genealogical thought at the intraspecific level (now formalized as coalescent theory) that these methods prompted. This paper traces the early history and explosive growth of phylogeography, and closes with predictions about future challenges for the field that centre on several facets of genealogical concordance.     

Molecular phylogeny of the antitropical subgenus Goniistius (Perciformes: Cheilodactylidae: Cheilodactylus): evidence for multiple transequatorial divergences and non-monophyly

The subgenus Goniistius comprises eight species of marine nearshore fishes which are antitropically distributed. The molecular phylogeny of these and other cheilodactylids was reconstructed from cytochrome oxidase I and cytochrome b mitochondrial DNA sequences. The placement within Goniistius of the morphologically divergent species Cheilodactylus (G.) nigripes was not supported. The remaining seven species are sufficiently divergent from other cheilodactylids to be designated as a separate genus. The antitropical distribution oi Goniistius is the result of three transequatorial divergences, which occurred during two periods. Based on molecular clock calibrations, these periods are suggested to be the mid Miocene, and late Miocene to early Pliocene. It is not known in which direction or by which mechanism these transequatorial divergences occurred, although biogeographic hypotheses of Mesozoic or Pleistocene separations can be discounted. The degree of genetic divergence between North and South Pacific populations of C. (G.) mttatus Garrett indicates that they have undergone cryptic speciation.     

Comparative mtDNA phylogeography of neotropical freshwater fishes: testing shared history to infer the evolutionary landscape of lower Central America

Historical biogeography seeks to explain contemporary distributions of taxa in the context of intrinsic biological and extrinsic geological and climatic factors. To decipher the relative importance of biological characteristics vs. environmental conditions, it is necessary to ask whether groups of taxa with similar distributions share the same history of diversification. Because all of the taxa will have shared the same climatic and geological history, evidence of shared history across multiple species provides an estimate of the role of extrinsic factors in shaping contemporary biogeographic patterns. Similarly, differences in the records of evolutionary history across species will probably be signatures of biological differences. In this study, we focus on inferring the evolutionary history for geographical populations and closely related species representing three genera of primary freshwater fishes that are widely distributed in lower Central America (LCA) and northwestern Colombia. Analysis of mitochondrial gene trees provides the opportunity for robust tests of shared history across taxa. Moreover, because mtDNA permits inference of the temporal scale of diversification we can test hypotheses regarding the chronological development of the Isthmian corridor linking North and South America. We have focused attention on two issues. First, we show that many of the distinct populations of LCA fishes diverged in a relatively brief period of time thus limiting the phylogenetic signal available for tests of shared history. Second, our results provide reduced evidence of shared history when all drainages are included in the analysis because of inferred dispersion events that obscure the evolutionary history among drainage basins. When we restrict the analysis to areas that harbour endemic mitochondrial lineages, there is evidence of shared history across taxa. We hypothesize that there were two to three distinct waves of invasion into LCA from putative source populations in northwestern Colombia. The first probably happened in the late Miocene, prior to the final emergence of the Isthmus in the mid-Pliocene; the second was probably coincident with the rise of the Isthmus in the mid-Pliocene, and the third event occurred more recently, perhaps in the Pleistocene. In each case the geographical scale of the dispersion of lineages was progressively more limited, a pattern we attribute to the continuing development of the landscape due to orogeny and the consequent increase in the insularization of drainage basins. Thus, the fisheye view of LCA suggests a complex biogeographic history of overlaid cycles of colonization, diversification, sorting and extinction of lineages.     

Comparative phylogeography of the western Indian Ocean reef fauna

Assessing patterns of connectivity at the community and population levels is relevant to marine resource management and conservation. The present study reviews this issue with a focus on the western Indian Ocean (WIO) biogeographic province. This part of the Indian Ocean holds more species than expected from current models of global reef fish species richness. In this study, checklists of reef fish species were examined to determine levels of endemism in each of 10 biogeographic provinces of the Indian Ocean. Results showed that the number of endemic species was higher in the WIO than in any other region of the Indian Ocean. Endemic species from the WIO on the average had a larger body size than elsewhere in the tropical Indian Ocean. This suggests an effect of peripheral speciation, as previously documented in the Hawaiian reef fish fauna, relative to other sites in the tropical western Pacific. To explore evolutionary dynamics of species across biogeographic provinces and infer mechanisms of speciation, we present and compare the results of phylogeographic surveys based on compilations of published and unpublished mitochondrial DNA sequences for 19 Indo-Pacific reef-associated fishes (rainbow grouper Cephalopholis argus, scrawled butterflyfish Chaetodon meyeri, bluespot mullet Crenimugil sp. A, humbug damselfish Dascyllus abudafur/Dascyllus aruanus, areolate grouper Epinephelus areolatus, blacktip grouper Epinephelus fasciatus, honeycomb grouper Epinephelus merra, bluespotted cornetfish Fistularia commersonii, cleaner wrasse Labroides sp. 1, longface emperor Lethrinus sp. A, bluestripe snapper Lutjanus kasmira, unicornfishes Naso brevirosris, Naso unicornis and Naso vlamingii, blue-spotted maskray Neotrygon kuhlii, largescale mullet Planiliza macrolepis, common parrotfish Scarus psicattus, crescent grunter Terapon jarbua, whitetip reef shark Triaenodon obesus) and three coastal Indo-West Pacific invertebrates (blue seastar Linckia laevigata, spiny lobster Panulirus homarus, small giant clam Tridacna maxima). Heterogeneous and often unbalanced sampling design, paucity of data in a number of cases, and among-species discrepancy in phylogeographic structure precluded any generalization regarding phylogeographic patterns. Nevertheless, the WIO might have been a source of haplotypes in some cases and it also harboured an endemic clade in at least one case. The present survey also highlighted likely cryptic species. This may eventually affect the accuracy of the current checklists of species, which form the basis of some of the recent advances in Indo-West Pacific marine ecology and biogeography.     

New species of tremstodes from Indian Ocean and Red Sea fishes

On the basis of the material collected in the Red Sea and the Indian Ocean four new species of trematodes are described: Bucephalopsis pseni sp. n., Diploproctodaeum chelonodoni sp. n., Bucephalus neoscombropsi sp. n., Phyllodistomum sobolevi sp. n. Anatomical and morphological characteristics of the above species as well as original figures of the trematodes are given, their taxonomic position is discussed.     

Incipient speciation of Catostylus mosaicus (Scyphozoa, Rhizostomeae, Catostylidae), comparative phylogeography and biogeography in south-east Australia

Aim Phylogeography provides a framework to explain and integrate patterns of marine biodiversity at infra‐ and supra‐specific levels. As originally expounded, the phylogeographic hypotheses are generalities that have limited discriminatory power; the goal of this study is to generate and test specific instances of the hypotheses, thereby better elucidating both local patterns of evolution and the conditions under which the generalities do or do not apply. Location Coastal south‐east Australia (New South Wales, Tasmania and Victoria), and south‐west North America (California and Baja California). Methods Phylogeographic hypotheses specific to coastal south‐east Australia were generated a priori, principally from existing detailed distributional analyses of echinoderms and decapods. The hypotheses are tested using mitochondrial cytochrome c oxidase subunit I (COI) and nuclear internal transcribed spacer 1 (ITS1) DNA sequence data describing population variation in the jellyfish Catostylus mosaicus, integrated with comparable data from the literature. Results Mitochondrial COI distinguished two reciprocally monophyletic clades of C. mosaicus (mean ± SD: 3.61 ± 0.40% pairwise sequence divergence) that were also differentiated by ITS1 haplotype frequency differences; the boundary between the clades was geographically proximate to a provincial zoogeographic boundary in the vicinity of Bass Strait. There was also limited evidence of another genetic inhomogeneity, of considerably smaller magnitude, in close proximity to a second hypothesized zoogeographic discontinuity near Sydney. Other coastal marine species also show genetic divergences in the vicinity of Bass Strait, although they are not closely concordant with each other or with reported biogeographic discontinuities in the region, being up to several hundreds of kilometres apart. None of the species studied to date show a strong phylogeographic discontinuity across the biogeographic transition zone near Sydney. Main conclusions Patterns of evolution in the Bass Strait and coastal New South Wales regions differ fundamentally because of long‐term differences in extrinsic factors. Since the late Pliocene, periods of cold climate and low sea‐level segregated warm temperate organisms east or west of an emergent Bassian Isthmus resulting in population divergence and speciation; during subsequent periods of warmer and higher seas, sister taxa expanded into the Bass Strait region leading to weakly correlated phylogeographic and biogeographic patterns. The Sydney region, by contrast, has been more consistently favourable to shifts in species’ ranges and long‐distance movement, resulting in a lack of intra‐specific and species‐level diversification. Comparisons between the Sydney and Bass Strait regions and prior studies in North America suggest that vicariance plays a key role in generating coastal biodiversity and that dispersal explains many of the deviations from the phylogeographic hypotheses.     

Phylogeography of colonially nesting seabirds, with special reference to global matrilineal patterns in the sooty tern (Sterna fuscata)

Sooty tern (Sterna fuscata) rookeries are scattered throughout the tropical oceans. When not nesting, individuals wander great distances across open seas, but, like many other seabirds, they tend to be site-faithful to nesting locales in successive years. Here we examine the matrilineal history of sooty terns on a global scale. Assayed colonies within an ocean are poorly differentiated in mitochondrial DNA sequence, a result indicating tight historical ties. However, a shallow genealogical partition distinguishes Atlantic from Indo-Pacific rookeries. Phylogeographic patterns in the sooty tern are compared to those in other colonially nesting seabirds, as well as in the green turtle (Chelonia mydas), an analogue of tropical seabirds in some salient aspects of natural history. Phylogeographic structure within an ocean is normally weak in seabirds, unlike the pronounced matrilineal structure in green turtles. However, the phylogeographic partition between Atlantic and Indo-Pacific rookeries in sooty terns mirrors, albeit in shallower evolutionary time, the major matrilineal subdivision in green turtles. Thus, global geology has apparently influenced historical gene movements in these two circumtropical species.     

A genetic metapopulation model for reef fishes in oceanic islands: the case of the surgeonfish,Acanthurus triostegus

Allozyme data on a surgeonfish, Acanthurus triostegus, were analysed from 10 islands in French Polynesia. We compared estimates of gene flow according to the hypothesis of an equilibrium between genetic drift and migration, and estimated genetic divergence times assuming complete genetic isolation without gene flow since foundation. The significant correlation between genetic divergence and geographic distance, at the within-archipelago level (r = 0.709, P = 0.024) indicates exchange of individuals mainly between neighbouring populations. The correlation was, however, not significant at the among-archipelagoes level (r = 0.325, P = 0.330), suggesting that long distance migrations are more sporadic. This addresses the problem of scale in population biology. According to the spatial scale of analysis, results can change from an island model, with no relation between genetic differentiation and geographical distances between archipelagos, to an isolation-by-distance model within an archipelago. These factors lead us to propose a “patchy population” model, in which all patches are occupied and reproductively active, though with few successful migrations between neighbouring populations. This model describes a subdivided population that is stable through time, with an amount of gene flow small enough to allow significant local differentiation in neutral gene frequency, but high enough to prevent differential fixation in the long term, and therefore preserving the genetic cohesion of the species.     

Evolution in caves: Darwin’s ‘wrecks of ancient life’ in the molecular era

Cave animals have historically attracted the attention of evolutionary biologists because of their bizarre ‘regressive’ characters and convergent evolution. However, understanding of their biogeographic and evolutionary history, including mechanisms of speciation, has remained elusive. In the last decade, molecular data have been obtained for subterranean taxa and their surface relatives, which have allowed some of the classical debates on the evolution of cave fauna to be revisited. Here, we review some of the major studies, focusing on the contribution of phylogeography in the following areas: biogeographic history and the relative roles of dispersal and vicariance, colonization history, cryptic species diversity and modes of speciation of cave animals. We further consider the limitations of current research and prospects for the future. Phylogeographic studies have confirmed that cave species are often cryptic, with highly restricted distributions, but have also shown that their divergence and potential speciation may occur despite the presence of gene flow from surface populations. Significantly, phylogeographic studies have provided evidence for speciation and adaptive evolution within the confines of cave environments, questioning the assumption that cave species evolved directly from surface ancestors. Recent technical developments involving ‘next generation’ DNA sequencing and theoretical developments in coalescent and population modelling are likely to revolutionize the field further, particularly in the study of speciation and the genetic basis of adaptation and convergent evolution within subterranean habitats. In summary, phylogeographic studies have provided an unprecedented insight into the evolution of these unique fauna, and the future of the field should be inspiring and data rich.     

Pan-European phylogeography of the aquatic snail Theodoxus fluviatilis (Gastropoda: Neritidae)

Investigating the geographical distribution of genetic lineages within species is critical to our understanding of how species evolve. As many species inhabit large and complex ranges, it is important that phylogeographical research take into account the entire range of widespread species to clarify how myriad extrinsic variables have affected their evolutionary history. Using phylogenetic, nested clade, and mismatch distribution analyses on a portion of the mitochondrial COI gene, I demonstrate that the wide-ranging freshwater snail Theodoxus fluviatilis possesses in parallel many of the phylogeographical patterns seen in less widespread freshwater species of Europe. Fragmentary forces play a major part in structuring the range of this species, with 12 of 14 geographically structured nested clades displaying a distribution consistent with fragmentation or restricted dispersal. Certain regions of southern Europe harbour the majority of genetic diversity (total haplotype diversity, H = 0.87), particularly Italy (H = 0.87) and areas surrounding the Black Sea (H = 0.81). Post-Pleistocene range expansion is pronounced, with the majority of northern European populations (95% of sample sites) having arisen from northern Italian individuals that initially colonized northern Germany. Additionally, two highly divergent haplotype lineages present in northern Germany imply that there were at least two postglacial recolonization routes. Estuaries may also provide a means of dispersal given that no genetic differentiation was found between estuarine populations and neighbouring freshwater populations. Taken together, these data reveal a species with a complex genetic history resulting from the fragmentary effects of European geology as well as continuous and discrete range expansion related to their aquatic biology.     

Comparative phylogeography and speciation of dung beetles from the Australian Wet Tropics rainforest

In tropical rainforests, insects show especially high species richness and local endemism of species relative to vertebrates. One possible cause is that insects respond to historical fluctuations of rainforests on a smaller spatial scale than do vertebrates. To evaluate this hypothesis, we combine environmental niche models and mitochondrial DNA phylogeography for two pairs of sister species of the dung beetle genus Temnoplectron (T. aeneopiceum-T. subvolitans and T. politulum-T. reyi) from the rainforests of northeastern Australia, where climate-driven rainforest fluctuations in the Quaternary have strongly influenced genetic and species diversity of vertebrates. Within both species pairs, the bioclimatic niche was conserved, but the T. aeneopiceum-T. subvolitans species pair had the narrower environmental range, and thus more restricted potential distribution. Coalescent analyses indicated Late Pliocene or Early Pleistocene divergences for both species pairs, and earlier speciation in (T. aeneopiceum-T. subvolitans) than in (T. politulum-T. reyi). Phylogeographic structure in (T. aeneopiceum-T. subvolitans) was more pronounced than in (T. politulum-T. reyi), with significant isolation-by-distance in the former species-pair only. Nested clade and coalescence analyses indicated local range expansions for the T. aeneopiceum-subvolitans species pair and range-wide expansion for both T. politulum and T. reyi. We suggest that stronger phylogeographic structure and earlier divergence in (T. aeneopiceum-T. subvolitans) than in (T. politulum-T. reyi) reflects a stronger influence of environmental barriers to gene flow under the present climate and greater sensitivity to warmer and drier periods of the Quaternary. The two species pairs evidently responded to Quaternary rainforest fluctuations at spatial scales similar to those seen within low-vagility species of vertebrate. Despite this similarity of scale, these insect lineages are reproductively isolated at parapatric boundaries, whereas analogous lineages of vertebrates often are not. We suggest that rapid evolution of genitalia may facilitate geographic speciation in rainforest beetles.     

Dispersal barriers and isolation among deep-sea mussel populations (Mytilidae: Bathymodiolus) from eastern Pacific hydrothermal vents

Deep-sea hydrothermal vent species are widely dispersed among habitat islands found along the global mid-ocean ridge system. We examine factors that affect population structure, gene flow and isolation in vent-endemic mussels of the genus Bathymodiolus from the eastern Pacific Ocean. Mussels were sampled from localities including the Galapagos Rift (GAR, 0 degrees 48' N; 86 degrees 10' W) and the East Pacific Rise (EPR, 13 degrees N to 32 degrees S latitude) across a maximum distance of 4900 km. The sampled range crossed a series of topographical features that interrupt linear aspects of the ridge system, and it encompassed regions of strong cross-axis currents that could impede along-axis dispersal of mussel larvae. Examinations of mitochondrial DNA sequences and allozyme variation revealed significant barriers to gene flow along the ridge axis. All populations from the GAR and EPR from 13 degrees N to 11 degrees S were homogeneous genetically and appeared to experience unimpeded high levels of interpopulational gene flow. In contrast, mussels from north and south of the Easter Microplate were highly divergent (4.4%), possibly comprising sister-species that diverged after formation of the microplate approximately 4.5 Ma. Strong cross-axis currents associated with inflated bathymetry of the microplate region may reinforce isolation across this region.     

Phylogeny and form in fishes: Genetic and morphometric characteristics of dragonets (Foetorepus sp.) do not align

Measures of biodiversity are often hindered by a lack of methodological practices that distinguish cryptic or morphologically similar cohabiting species. This is particularly difficult for marine fishes where direct observations of the ecology and demography of populations are difficult. Dragonets (Foetorepus c.f. calauropomus) were collected as bycatch from research trawls deployed in waters off north-eastern Tasmania, Australia. Morphometric and genetic analyses were conducted on the 43 specimens recovered. Sequence analysis of two mitochondrial loci distinguished three genetic clusters, each having levels of dissimilarity consistent with species-level distinctions between other members of the Callionymidae. While clear morphological distinctions were observed between male and female fish, limited morphometric analyses could not differentiate between members of the three genetic groups. This finding highlights questions about the ability of genetically distinct but morphologically similar groups to occupy the same ecological niche, and points to additional and undescribed hidden biodiversity amongst cryptic species of fish.     

Small body size increases the regional differentiation of populations of tropical mantellid frogs (Anura: Mantellidae)

The processes affecting species diversification may also exert an influence on patterns of genetic variability within species. We evaluated the contributions of five variables potentially influencing clade diversification (body size, reproductive mode, range size, microhabitat and skin texture) on mtDNA divergence and polymorphism among populations of 40 species of frogs (Mantellidae) from two rainforest communities in Madagascar. We report an inverse association between body size and nucleotide divergence between populations but find no influence of other variables on genetic variation. Body size explained ca. 11% of the variation in nucleotide divergence between populations and was coupled with high F_ST levels and an absence of haplotype sharing in small‐bodied and medium‐sized frogs. Low dispersal ability is likely the proximate mechanism producing higher population differentiation in small mantellids. The lack of genetic cohesion among populations establishes regional genetic fragmentation which in turn has the potential to accelerate rates of allopatric speciation in small frogs relative to large species. However, there is little evidence of increased speciation rates in these or other small‐bodied organisms. We reconcile these contradictory observations by suggesting that lower dispersal ability also curbs colonization of new areas, decelerating diversification in weak dispersers. Our results imply that the intermediate dispersal model also applies to amphibians and may explain inconsistent previous results on the correlation of body size and speciation rate.