Peripheral Speciation Research Articles

Morphometric and Molecular Evidence Delimit Six Species in Clematis reticulata s.l. (Ranunculaceae: Clematis subg. Viorna)

Abstract— Clematis subgenus Viorna of North America currently consists of 21 species with most of the diversity found in the southeastern United States. Past taxonomic treatments of Clematis subg. Viorna have varied greatly, which has led to unclear species limits across multiple species complexes. Often recognized as a single, polymorphic species with a high degree of ecological amplitude, variation in the Clematis reticulata species complex has previously been attributed to phenotypic plasticity. A combination of herbarium specimen examination and extensive fieldwork led to the formation of seven a priori morphological groups, or hypothesized taxa, in the C. reticulata species complex based on previously used and novel morphological characters. We employ an integrative approach to species delimitation with data from morphometric studies of herbarium and common garden datasets, as well as a phylogeny inferred from ddRADseq. Of the seven hypothesized taxa, six were supported by evidence from morphology and phylogeny with corroborating biogeography and ecology. Recognition of Clematis terminalis sp. nov. renders C. subreticulata comb. nov. paraphyletic. Because of its morphological, ecological, and phenological distinctiveness, it may represent a case of peripheral speciation by isolation. Four new species are recognized: C. arenicola sp. nov., C. cumberlandensis sp. nov., C. ouachitensis sp. nov., and C. terminalis sp. nov. Viorna subreticulata is given a new combination in Clematis and the newly defined C. reticulata s.s. is re-circumscribed. An updated dichotomous key, species descriptions, ecological notes, and distribution maps are provided.

Mechanisms of peripheral phylogeographic divergence in the indo-Pacific: lessons from the spiny lobster Panulirus homarus

BackgroundThere is increasing recognition of the concordance between marine biogeographic and phylogeographic boundaries. However, it is still unclear how population-level divergence translates into species-level divergence, and what are the principal factors that first initiate that divergence, and then maintain reproductive isolation. This study examines the likely forces driving population and lineage divergences in the broadly-distributed Indo-Pacific spiny lobster Panulirus homarus, which has peripheral divergent lineages in the west and east. The study focuses particularly on the West Indian Ocean, which is emerging as a region of unexpected diversity. Mitochondrial control region (mtCR) and COI sequences as well as genotypes of 9 microsatellite loci were examined in 410 individuals from 17 locations grouped into 7 regions from South Africa in the west, and eastward across to Taiwan and the Marquesas Islands. Phylogenetic and population-level analyses were used to test the significance and timing of divergences and describe the genetic relationships among populations.ResultsAnalyses of the mtCR revealed high levels of divergence among the seven regions (ФST = 0.594, P < 0.001). Microsatellite analyses also revealed significant divergence among regions, but at a much lower level (FST = 0.066, P < 0.001). The results reveal different patterns of mtCR v. nDNA divergence between the two distinct peripheral lineages: a subspecies in South Africa and Madagascar, and a phylogeographically diverged population in the Marquesas. The results also expose a number of other more fine-scale population divergences, particularly in the Indian Ocean.ConclusionsThe divergence of peripheral lineages in the west and east of the species’ range appear to have been initiated and maintained by very different processes. The pattern of mitochondrial and nuclear divergence of the western lineage, implicates processes of parapatric isolation, secondary contact and introgression, and suggests possible maintenance through adaptation and behavioural reproductive isolation. In contrast, the eastern lineage appears to have diverged through a rare colonisation event, maintained through long-term isolation, and matches expectations of the core-periphery hypothesis. The process of active peripheral speciation may be a common force in the Indo-Pacific that helps drive some of the regions’ recognized biogeographic boundaries.

Phylogenetic perspectives on reef fish functional traits.

Functional traits have been fundamental to the evolution and diversification of entire fish lineages on coral reefs. Yet their relationship with the processes promoting speciation, extinction and the filtering of local species pools remains unclear. We review the current literature exploring the evolution of diet, body size, water column use and geographic range size in reef-associated fishes. Using published and new data, we mapped functional traits on to published phylogenetic trees to uncover evolutionary patterns that have led to the current functional diversity of fishes on coral reefs. When examining reconstructed patterns for diet and feeding mode, we found examples of independent transitions to planktivory across different reef fish families. Such transitions and associated morphological alterations may represent cases in which ecological opportunity for the exploitation of different resources drives speciation and adaptation. In terms of body size, reconstructions showed that both large and small sizes appear multiple times within clades of mid-sized fishes and that extreme body sizes have arisen mostly in the last 10 million years (Myr). The reconstruction of range size revealed many cases of disparate range sizes among sister species. Such range size disparity highlights potential vicariant processes through isolation in peripheral locations. When accounting for peripheral speciation processes in sister pairs, we found a significant relationship between labrid range size and lineage age. The diversity and evolution of traits within lineages is influenced by trait-environment interactions as well as by species and trait-trait interactions, where the presence of a given trait may trigger the development of related traits or behaviours. Our effort to assess the evolution of functional diversity across reef fish clades adds to the burgeoning research focusing on the evolutionary and ecological roles of functional traits. We argue that the combination of a phylogenetic and a functional approach will improve the understanding of the mechanisms of species assembly in extraordinarily rich coral reef communities.

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.

Blinded by the bright: a lack of congruence between colour morphs, phylogeography and taxonomy for a cosmopolitan Indo‐Pacific butterflyfish, Chaetodon auriga

AbstractAimWe assess genetic differentiation among biogeographical provinces and colour morphs of the threadfin butterflyfish, Chaetodon auriga. This species is among the most broadly distributed butterflyfishes in the world, occurring on reefs from the Red Sea and western Indian Ocean to French Polynesia and Hawai'i. The Red Sea form lacks a conspicuous ‘eye‐spot’ on the dorsal fin, which may indicate an evolutionary distinction.LocationRed Sea, Indian Ocean and Pacific Ocean.MethodsSpecimens were obtained at 17 locations (n = 358) spanning the entire range of this species. The genetic data included 669 base pairs of mitochondrial DNA (mtDNA) cytochrome b and allele frequencies at six microsatellite loci. Analysis of molecular variance, structure plots, haplotype networks and estimates of population expansion time were used to assess phylogeographical patterns.ResultsPopulation structure was low overall, but significant and concordant between molecular markers (mtDNA: ΦST = 0.027, P &lt; 0.001; microsatellites: FST = 0.023, P &lt; 0.001). Significant population‐level partitions were only detected at peripheral locations including the Red Sea and Hawai'i. Population expansion events in the Red Sea and Socotra are older (111,940–223,881 years) relative to all other sites (16,343–87,910 years).Main conclusionsWe find little genetic evidence to support an evolutionary partition of a previously proposed Red Sea subspecies. The oldest estimate of population expansion in the Red Sea and adjacent Gulf of Aden indicates a putative refuge in this region during Pleistocene glacial cycles. The finding of population separations at the limits of the range, in the Red Sea and Hawai'i, is consistent with peripheral speciation.

On the relationship between species age and geographical range in reef fishes: are widespread species older than they seem?

AbstractAimIn order to better understand processes of speciation, range‐size transformation and extinction, macroecological studies seek to identify the evolutionary dynamics of species geographical ranges. This requires accurate estimates of range size and species age. Species ages are attainable through recent success with techniques to estimate phylogenetic divergence time. Conceptual synthesis of the inherent problems with these techniques has been limited. Our aim is to address the effects of estimation of phylogenetic divergence time on the relationship between species age and geographical range.InnovationCommonly, estimates of divergence time from the nodes of a time‐calibrated phylogeny are used as indicators of ages of extant species. However, this method can sometimes produce misleading age estimates, specifically in the presence of extinction and ancestral persistence. An example of this is illustrated using a comprehensive genetic dataset of genera with near‐complete sampling of species from four of the major coral reef fish families. We present a method to minimize the impacts of extinction and ancestral persistence on divergence time estimation. The method focuses on recent divergences and involves pairing minimum divergence time estimates (as indicators of species ages) with the minimum geographical range area between two sister‐species, for all sister‐species pairs.Main conclusionsWhen applied to coral reef fishes, this method revealed trends in the relationship between species age and geographical range. The difference in the trend recovered from excluding potential biases associated with ancestral persistence suggests that ancestral persistence may be prevalent among coral reef fishes, with successive peripheral speciation affecting area–age relationships. The method may reveal the occurrence of successive peripheral speciation events across a broad range of taxa.

Spatiotemporal variation in morphological evolution in the Oligocene–Recent larger benthic foraminifera genus Cycloclypeus reveals geographically undersampled speciation

Accurate assessment of location and timing of speciation of species is needed to discriminate between macroevolutionary models explaining large scale biodiversity patterns. In this paper I evaluate fossil evidence of variation in geographical ranges through time, as well as spatio-temporal variation in morphological parameters to examine geographical aspects of speciation and range variation. Specifically I test for geographical morphological stability within time slices and for temporal modes of morphological change within lineages.Past distribution ranges of all species of the large benthic foraminifera Cycloclypeus have been documented on paleogeographic maps. From those samples with sufficiently well preserved specimens internal morphological data were measured and analysed.Within a small sample of six species in a single genus of reef associated large benthic foraminifera evidence for heterogeneity in geographic speciation modes, including vicariance, peripheral speciation, and sympatric speciation in the centre of the range has been found. Morphological evolution was found to be either homogeneous over large geographic ranges or spatially restricted. In time two gradually evolving lineages were found. Furthermore, an evolutionary transition of two species that previously was regarded as gradual, is shown to be punctuated with intermediate populations occurring restricted in both time and space.I demonstrate the marked heterogeneity of evolutionary processes and the difficulty to make assumptions regarding tempo and mode of evolution. Furthermore, I introduce the concept of geographically undersampled punctuations. This example exposes some of the pitfalls when conclusions regarding the mode and location of speciation are based on the combination of phylogeny and extant distribution alone.

Australasian sky islands act as a diversity pump facilitating peripheral speciation and complex reversal from narrow endemic to widespread ecological supertramp.

The Australasian archipelago is biologically extremely diverse as a result of a highly puzzling geological and biological evolution. Unveiling the underlying mechanisms has never been more attainable as molecular phylogenetic and geological methods improve, and has become a research priority considering increasing human-mediated loss of biodiversity. However, studies of finer scaled evolutionary patterns remain rare particularly for megadiverse Melanesian biota. While oceanic islands have received some attention in the region, likewise insular mountain blocks that serve as species pumps remain understudied, even though Australasia, for example, features some of the most spectacular tropical alpine habitats in the World. Here, we sequenced almost 2 kb of mitochondrial DNA from the widespread diving beetle Rhantus suturalis from across Australasia and the Indomalayan Archipelago, including remote New Guinean highlands. Based on expert taxonomy with a multigene phylogenetic backbone study, and combining molecular phylogenetics, phylogeography, divergence time estimation, and historical demography, we recover comparably low geographic signal, but complex phylogenetic relationships and population structure within R. suturalis. Four narrowly endemic New Guinea highland species are subordinated and two populations (New Guinea, New Zealand) seem to constitute cases of ongoing speciation. We reveal repeated colonization of remote mountain chains where haplotypes out of a core clade of very widespread haplotypes syntopically might occur with well-isolated ones. These results are corroborated by a Pleistocene origin approximately 2.4 Ma ago, followed by a sudden demographic expansion 600,000 years ago that may have been initiated through climatic adaptations. This study is a snapshot of the early stages of lineage diversification by peripatric speciation in Australasia, and supports New Guinea sky islands as cradles of evolution, in line with geological evidence suggesting very recent origin of high altitudes in the region.

Habitat Availability and Heterogeneity and the Indo-Pacific Warm Pool as Predictors of Marine Species Richness in the Tropical Indo-Pacific

Range overlap patterns were observed in a dataset of 10,446 expert-derived marine species distribution maps, including 8,295 coastal fishes, 1,212 invertebrates (crustaceans and molluscs), 820 reef-building corals, 50 seagrasses, and 69 mangroves. Distributions of tropical Indo-Pacific shore fishes revealed a concentration of species richness in the northern apex and central region of the Coral Triangle epicenter of marine biodiversity. This pattern was supported by distributions of invertebrates and habitat-forming primary producers. Habitat availability, heterogeneity, and sea surface temperatures were highly correlated with species richness across spatial grains ranging from 23,000 to 5,100,000 km2 with and without correction for autocorrelation. The consistent retention of habitat variables in our predictive models supports the area of refuge hypothesis which posits reduced extinction rates in the Coral Triangle. This does not preclude support for a center of origin hypothesis that suggests increased speciation in the region may contribute to species richness. In addition, consistent retention of sea surface temperatures in models suggests that available kinetic energy may also be an important factor in shaping patterns of marine species richness. Kinetic energy may hasten rates of both extinction and speciation. The position of the Indo-Pacific Warm Pool to the east of the Coral Triangle in central Oceania and a pattern of increasing species richness from this region into the central and northern parts of the Coral Triangle suggests peripheral speciation with enhanced survival in the cooler parts of the Coral Triangle that also have highly concentrated available habitat. These results indicate that conservation of habitat availability and heterogeneity is important to reduce extinction of marine species and that changes in sea surface temperatures may influence the evolutionary potential of the region.

THE EVOLUTION OF ENDEMISM IN INSULAR PACIFIC FAUNAS: CORAL-DWELLING STOMATOPODS

Coral-dwelling stomatopods, as well as other groups of marine invertebrates, are dwarfed on Pacific atolls compared to high island or mainland faunas. Particularly on atolls, typical body size diminishes progressively within lineages and among assemblages of species as one moves eastward from the Austral-Asian continental region of highest diversity toward the mid-Pacific, which is a region of high endemism. Populations on atolls are particularly diminutive. Lower productivity in the Central Pacific than on the Indo-West Pacific continental shelf and lower productivity on atolls compared to high islands may explain this pattern. In the mid-Pacific, however, smaller body sizes result in fewer, smaller, less well-dispersing offspring, trapping the lineage as a endemic. Dispersal from the large species on the Austral-Asian continental area appears to dampen differentiation in the adjacent West Pacific region, which is characterized by low endemism. The East Indies center of origin and the peripheral speciation models are not mutually exclusive, however, since the Austral-Asian continental seas are inhabited by both large and small species, and endemism among small lineages is even higher in the Indo-West Pacific continental region than in the areas. Here, biotic factors associated with competition for refuges may have selected for small species that can exploit the much more numerous small refuges in the reef, while the pugnacious larger species follow a riskier and energetically expensive path, fighting viciously for increasingly rare large holes in the calcareous substrate in order to reap the temitorial and reproductive benefits that result from large body size.

Molecular biogeography of the Pacific

Species-range information forms the empirical data base for much of biogeography, but even with a huge amount of data on species occurrences, many of the ecological and evolutionary processes generating biogeographic patterns remain obscure. Molecular genetic data from closely related, widely distributed species can help address biogeographic mechanisms by (1) providing independent evidence for genetic boundaries between cryptic species, (2) estimating species divergence times, (3) providing phylogenetic reconstructions of species divergence patterns, and (4) allowing us to examine the geography of allelic variants within species and ask if intra-specific alleles show the same biogeographic patterns as do species. Data from mitochondrial DNA variation in Pacific sea urchins and butterfly fishes show that congeneric species diverged within the Pleistocene. Thus, the processes that generate species diversity patterns probably have been acting throughout the recent past, and are ongoing aspects of Pacific marine biology. Phylogenetic analysis of mtDNA variants suggests that sea urchin species arise throughout the Pacific, with some originating by peripheral speciation and some evolving in the high diversity center of the Indo-West Pacific. Clines of mtDNA variation within species are similar to diversity clines in the entire fauna. Similar biogeographic patterns for species and for alleles within species may provide unique clues about the processes that generate biological diversity both within and between species.