Congruent phylogeographic patterns in a young radiation of live‐bearing marine snakes: Pleistocene vicariance and the conservation implications of cryptic genetic diversity

Aim

To investigate phylogeographic patterns among and within co‐occurring sea snake species from Australia's endemic viviparous Aipysurus lineage, which includes critically endangered species, and evaluate the conservation implications of geographically structured patterns of genetic divergence and diversity.

Location

Australia's tropical shallow water marine environments spanning four regions: Great Barrier Reef (GBR), Gulf of Carpentaria (GoC), Timor Sea (TS) and coastal WA (WAC).

Methods

Samples from >550 snakes representing all nine nominal Aipysurus group species were obtained from throughout their known Australian ranges. Coalescent phylogenetic analyses and Bayesian molecular dating of mitochondrial DNA, combined with Bayesian and traditional population genetic analyses of 11 microsatellite loci, were used to evaluate genetic divergence and diversity.

Results

Mitochondrial DNA revealed highly congruent phylogeographic breaks among co‐occurring species, largely supported by nuclear microsatellites. For each species, each region was characterized by a unique suite of haplotypes (phylogroups). Divergences between the TS, GoC and/or GBR were invariably shallow and dated as occurring 50,000–130,000 years ago, coinciding with the cyclic Pleistocene emergence of the Torres Strait land bridge. By contrast, sea snakes from coastal WA were consistently highly divergent from other regions and dated as diverging 178,000–526,000 years ago, which was not associated with any known vicariant events.

Main Conclusions

Previously unappreciated highly divergent sea snake lineages in coastal WA potentially represent cryptic species, highlighting this region as a high‐priority area for conservation. The cyclic emergence of the Torres Strait land bridge is consisted with observed divergences between the TS, GoC and/or GBR; however, processes involved in the earlier divergences involving the WAC remain to be determined. The observed strong population genetic structures (as surrogates for dispersal) indicate that sea snakes have limited potential to reverse population declines via replenishment from other sources over time frames relevant to conservation.

     

Panbiogeography of New Caledonia,south‐west Pacific: basal angiosperms on basement terranes,ultramafic endemics inherited from volcanic island arcs and old taxa endemic to young islands

Aim To investigate areas of endemism in New Caledonia and their relationship with tectonic history. Location New Caledonia, south‐west Pacific. Methods Panbiogeographical analysis. Results Biogeographical patterns within New Caledonia are described and illustrated with reference to eight terranes and ten centres of endemism. The basement terranes make up a centre of endemism for taxa including Amborella, the basal angiosperm. Three of the terranes that accreted to the basement in the Eocene (high‐pressure metamorphic terrane, ultramafic nappe and Loyalty Ridge) have their own endemics. Main conclusions New Caledonia is not simply a fragment of Gondwana but, like New Zealand and New Guinea, is a complex mosaic of allochthonous terranes. The four New Caledonian basement terranes were all formed from island arc‐derived and arc‐associated material (including ophiolites) which accumulated in the pre‐Pacific Ocean, not in Gondwana. They amalgamated and were accreted to Gondwana (eastern Australia) in the Late Jurassic/Early Cretaceous, but in the Late Cretaceous they separated from Australia with the opening of the Tasman Sea and break‐up of Gondwana. An Eocene collision of the basement terranes with an island arc to the north‐east – possibly the Loyalty Ridge – is of special biogeographical interest in connection with New Caledonia–central Pacific affinities. The Loyalty–Three Kings Ridge has had a separate history from that of the Norfolk Ridge/New Caledonia, although both now run in parallel between Vanuatu and New Zealand. The South Loyalty Basin opened between Grande Terre and the Loyalty Ridge in the Cretaceous and attained a width of 750 km. However, it was almost completely destroyed by subduction in the Eocene which brought the Loyalty Ridge and Grande Terre together again, after 30 Myr of separation. The tectonic history is reflected in the strong biogeographical differences between Grande Terre and the Loyalty Islands. Many Loyalty Islands taxa are widespread in the Pacific but do not occur on Grande Terre, and many Grande Terre/Australian groups are not on the Loyalty Islands. The Loyalty Islands are young (2 Myr old) but they are merely the currently emergent parts of the Loyalty Ridge whose ancestor arcs have a history of volcanism dating back to the Cretaceous. Old taxa endemic to the young Loyalty Ridge islands persist over geological time as a dynamic metapopulation surviving in situ on the individually ephemeral islands and atolls found around subduction zones. The current Loyalty Islands, like the Grande Terre terranes, have inherited their biota from previous islands. On Grande Terre, the ultramafic terrane was emplaced on Grande Terre in the Eocene (about the same time as the collision with the island arc). The very diverse endemic flora on the ultramafics may have been inherited by the obducting nappe from prior base‐rich habitat in the region, including the mafic Poya terrane and the limestones typical of arc and intraplate volcanic islands.     

Seamounts: centres of endemism or species richness for ophiuroids?

Aim To test the hypotheses that seamounts exhibit high rates of endemism and/or species richness compared to surrounding areas of the continental slope and oceanic ridges. Location The south‐west Pacific Ocean from 19–57° S to 143–171° E. Methods Presence/absence museum data were compiled for seamount and non‐seamount areas at depths between 100 and 1500 m for the Ophiuroidea (brittle‐stars), an abundant and speciose group of benthic invertebrates. Large‐scale biogeographical gradients were examined through multivariate analyses at two spatial scales, at the scale of seamounts (< 1° of latitude/longitude) and regions (5–9°). The robustness of these patterns to spatially inconsistent sampling effort was tested using Monte Carlo‐style simulations. Levels of local endemism and species richness over numbers of samples were compared for seamount and non‐seamount areas using linear regressions. Non‐seamount populations were randomly generated from areas and depth ranges that reflected the typical sampling profile of seamounts. Results Seamount ophiuroid assemblages did not exhibit elevated levels of species richness or narrow‐range endemism compared with non‐seamount areas. Seamounts can exhibit high overall species richness for low numbers of samples, particularly on seamounts supporting a dense coral matrix, but this does not increase with additional sampling at the rates found in non‐seamount areas. There were relatively few identifiable seamount specialists. In general, seamount faunas reflected those found at similar depths in surrounding areas, including the continental slope. Seamount and non‐seamount faunas within the study area exhibited congruent latitudinal and bathymetric species turnover. Main conclusions Seamount faunas were variable for ophiuroid faunal composition, species richness and narrow‐range endemism, reflecting their environmental diversity and complex history. The continental slope was also variable, with some areas being particularly species rich. Broad geomorphological habitat categories such as ‘seamounts’ or ‘continental slope’ may be at the wrong scale to be useful for conservation planning.     

Distribution, endemism and threat status of freshwater fishes in the Western Ghats of India

Aim To study (1) the large-scale distribution patterns of freshwater fishes in the Western Ghats of India; (2) the endemism and uniqueness of the fishes in various zones; and (3) the threat status of fishes by categorizing them under low risk (LR), vulnerable (VU), endangered (EN) and critically endangered (CR). Location The Western Ghats of India. Methods The scientific literature describing the freshwater fishes of the Western Ghats was reviewed. Data describing the lists of the species were extracted and complied. The species accumulation curve was plotted using Michaelis–Menten-like equation. The Western Ghats was divided into six zones and similarity of the species was calculated using Jacquard's index. Results Literature to date records 288 species belonging to 12 orders, 41 families and 109 genera, of which 118 species are endemic and 51 are unique. However, the species accumulation curve shows that there might be 345 species in this region, indicating that 16% species have not been recorded to date. An analysis of the distribution pattern of fishes in the Western Ghats suggests that the southern region is more diverse than the northern and central regions. The southern region shows high endemism and high uniqueness while the northern region shows high endemism but less uniqueness. The similarity index between the zones indicates that as the distance between the zones increases similarity decreases. The status of 105 of 288 species was not known due to data deficiency but among the remaining 183 species, 58 species were categorized as LR, 41 as VU, 54 as EN, 24 as CR while the remaining six species were introduced. Conclusions The distribution patterns of fishes in the Western Ghats are discussed in accordance with the geography of Western Ghats, its climatic conditions and ‘Satpura Hypothesis’. The threat status of fishes found in Western Ghats suggests that at least 41% of fish fauna is threatened by either being VU, EN or CR. Implication of potent conservation measures is necessary to conserve the fish fauna of Western Ghats.     

Contrasting genetic diversity and population structure among three sympatric Madagascan shorebirds: parallels with rarity,endemism, and dispersal

Understanding the relative contributions of intrinsic and extrinsic factors to population structure and genetic diversity is a central goal of conservation and evolutionary genetics. One way to achieve this is through comparative population genetic analysis of sympatric sister taxa, which allows evaluation of intrinsic factors such as population demography and life history while controlling for phylogenetic relatedness and geography. We used ten conserved microsatellites to explore the population structure and genetic diversity of three sympatric and closely related plover species in southwestern Madagascar: Kittlitz's plover (Charadrius pecuarius), white‐fronted plover (C. marginatus), and Madagascar plover (C. thoracicus). Bayesian clustering revealed strong population structure in the rare and endemic Madagascar plover, intermediate population structure in the white‐fronted plover, and no detectable population structure in the geographically widespread Kittlitz's plover. In contrast, allelic richness and heterozygosity were highest for the Kittlitz's plover, intermediate for the white‐fronted plover and lowest for the Madagascar plover. No evidence was found in support of the “watershed mechanism” proposed to facilitate vicariant divergence of Madagascan lemurs and reptiles, which we attribute to the vagility of birds. However, we found a significant pattern of genetic isolation by distance among populations of the Madagascar plover, but not for the other two species. These findings suggest that interspecific variation in rarity, endemism, and dispersal propensity may influence genetic structure and diversity, even in highly vagile species.     

Assessing biodiversity and endemism using phylogenetic methods across multiple taxonomic groups

Identifying geographical areas with the greatest representation of the tree of life is an important goal for the management and conservation of biodiversity. While there are methods available for using a single phylogenetic tree to assess spatial patterns of biodiversity, there has been limited exploration of how separate phylogenies from multiple taxonomic groups can be used jointly to map diversity and endemism. Here, we demonstrate how to apply different phylogenetic approaches to assess biodiversity across multiple taxonomic groups. We map spatial patterns of phylogenetic diversity/endemism to identify concordant areas with the greatest representation of biodiversity across multiple taxa and demonstrate the approach by applying it to the Murray–Darling basin region of southeastern Australia. The areas with significant centers of phylogenetic diversity and endemism were distributed differently for the five taxonomic groups studied (plant genera, fish, tree frogs, acacias, and eucalypts); no strong shared patterns across all five groups emerged. However, congruence was apparent between some groups in some parts of the basin. The northern region of the basin emerges from the analysis as a priority area for future conservation initiatives focused on eucalypts and tree frogs. The southern region is particularly important for conservation of the evolutionary heritage of plants and fishes.     

Phylogeny and vicariant speciation of the Grey Rhebok,Pelea capreolus

A South African endemic antelope, the Grey Rhebok (Pelea capreolus), has long been an evolutionary enigma in bovid systematics—its phylogenetic intractability attributed to its curious combination of derived and primitive morphological attributes and the consequences of a rapid radiation. By using a combination of DNA sequences, chromosomal characteristics and quantitative and qualitative morphological features we show that the species is a sister taxon to a clade that comprises the waterbuck, reedbuck and allies. Our finding of few unambiguous synapomorphies reinforces suggestions of a rapid radiation and highlights the effects of incomplete lineage sorting, including the hemiplasic nature of several chromosomal rearrangements. We investigate these data to address the general question of what may have led to Pelea being both genetically and ecologically distinct from the Reduncini. We argue that its adaptation to exposed habitats, free of standing water, arose by vicariance prompted by increasing aridity of the extreme south/southwestern region of the African continent in the Miocene. Ancestral lineages leading to the extant Redunca and Kobus, on the other hand, retreated to water-abundant refugia in the north during these mostly globally cool phases. The mosaic of water-rich environments provided by the Okavango and the drainage systems in the southwestern extension of the East African Rift system are considered to have facilitated speciation and chromosomal evolution within these antelope.     

Disentangling the drivers of continental mammalian endemism

Endemic species and species with small ranges are ecologically and evolutionarily distinct and are vulnerable to extinction. Determining which abiotic and biotic factors structure patterns of endemism on continents can advance our understanding of global biogeographic processes, but spatial patterns of mammalian endemism have not yet been effectively predicted and reconstructed. Using novel null model techniques, we reconstruct trends in mammalian endemism and describe the isolated and combined effects of physiographic, ecological, and evolutionary factors on endemism. We calculated weighted endemism for global continental ecoregions and compared the spatial distribution of endemism to niche-based, geographic null models of endemism. These null models distribute species randomly across continents, simulating their range sizes from their degree of climatic specialization. They isolate the effects of physiography (topography and climate) and species richness on endemism. We then ran linear and structural models to determine how topography and historical climate stability influence endemism. The highest rates of mammalian endemism were found in topographically rough, climatically stable ecoregions with many species. The null model that isolated physiography did not closely approximate the observed distribution of endemism (r² = .09), whereas the null model that incorporated both physiography and species richness did (r² = .59). The linear models demonstrate that topography and climatic stability both influenced endemism values, but that average climatic niche breadth was not highly correlated with endemism. Climate stability and topography both influence weighted endemism in mammals, but the spatial distribution of mammalian endemism is driven by a combination of physiography and species richness. Despite its relationship to individual range size, average climate niche breadth has only a weak influence on endemism. The results highlight the importance of historical biogeographic processes (e.g. centers of speciation) and geography in driving endemism patterns, and disentangle the mechanisms structuring species ranges worldwide.     

Hidden areas of endemism: Small units in the South-eastern Neotropics

This study aimed to establish if the Lower Río de la Plata Basin (LRPB) wetlands can be considered a biogeographic unit. The species of this area were compiled and segregated according to the habitat, selecting only 87 endemic taxa restricted to the LRPB and linked to wetlands. Distributional data of species obtained from the literature, web databases, biological collections, and field trips were georeferenced. The areas of endemism were established as those areas where the distribution of two or more taxa overlaps in groups of rivers’ sections with geographic continuity and were tested with a cluster analysis. This congruence is due to ecological, geomorphological, and historical factors. Four areas of endemism were found: a broad area that comprises the whole study area (Riverine district), which is divided into three nested smaller areas (Paraguay–Paraná Flooding Valleys, Uruguay Basin, and Paraná Delta subdistricts). Then, we analysed 170 taxa distributions to evaluate the relationship between the study area and the neighbouring biogeographic units. According to the results, the study area belongs to the Paraná biogeographic province. Some areas of endemism are hidden inside broader areas and are hardly detected with the currently used biogeographic grid-methods. We propose to combine the information about ecological requirements of each taxon with its georeferenced records to estimate their areas of distribution as a primary step for searching areas of endemism in intracontinental studies.