Cryptic biodiversity in a changing world

DNA studies are revealing the extent of hidden, or cryptic, biodiversity. Two new studies challenge paradigms about cryptic biodiversity and highlight the importance of adding a historical and biogeographic dimension to biodiversity research

Towards population-level conservation in the critically endangered Antarctic blue whale: the number and distribution of their populations

This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/Population-level conservation is required to prevent biodiversity loss within a species, but it first necessitates determining the number and distribution of populations. Many whale populations are still depleted due to 20th century whaling. Whales are one of the most logistically difficult and expensive animals to study because of their mobility, pelagic lifestyle and often remote habitat. We tackle the question of population structure in the Antarctic blue whale (Balaenoptera musculus intermedia) – a critically endangered subspecies and the largest extant animal – by capitalizing on the largest genetic dataset to date for Antarctic blue whales. We found evidence of three populations that are sympatric in the Antarctic feeding grounds and likely occupy separate breeding grounds. Our study adds to knowledge of population structure in the Antarctic blue whale. Future research should invest in locating the breeding grounds and migratory routes of Antarctic blue whales through satellite telemetry to confirm their population structure and allow population-level conservation

Alternative conservation outcomes from aquatic fauna translocations: Losing and saving the Running River rainbowfish

1. The translocation of species outside their natural range is a threat to aquatic biodiversity globally, especially freshwater fishes, as most are not only susceptible to predation and competition but readily hybridize with congeners. 2. Running River rainbowfish (RRR, Melanotaenia sp.) is a narrow-ranged, small-bodied freshwater fish that recently became threatened and was subsequently listed as Critically Endangered, owing to introgressive hybridization and competition following the translocation of a congeneric species, the eastern rainbowfish (Melanotaenia splendida). 3. To conserve RRR, wild fish were taken into captivity, genetically confirmed as pure representatives, and successfully bred. As the threat of introgression with translocated eastern rainbowfish could not be mitigated, a plan was devised to translocate captive raised RRR into unoccupied habitats within their native catchment, upstream of natural barriers. The translocation plan involved careful site selection and habitat assessment, predator training (exposure to predators prior to release), soft release (with a gradual transition from captivity to nature), and post-release monitoring, and this approach was ultimately successful. 4. Two populations of RRR were established in two previously unoccupied streams above waterfalls with a combined stream length of 18 km. Post-release monitoring was affected by floods and low sample sizes, but suggested that predation and time of release are important factors to consider in similar conservation recovery programmes for small-bodied, short-lived fishes

Genetic characterization of native and introduced populations of the neotropical cichlid genus Cichla in Brazil

A molecular phylogenetic analysis based on mitochondrial 16S ribosomal DNA and Control Region sequences from native and introduced populations was undertaken, in order to characterize the introduction of Cichla (peacock bass or tucunaré) species in Brazil. Mitochondrial DNA haplotypes found in introduced fish from Minas Gerais state (southeastern Brazil) clustered only with those from native species of the Tocantins River (Cichla piquiti and C. kelberi), thereby suggesting a single or, at most, few translocation acts in this area, even though with fish from the same source-population. Our study contributes to an understanding of the introduction of Cichla in regions of Brazil outside the Amazon basin, and adds phylogenetic data to the recently describe Cichla species, endemic from the Tocantins-Araguaia basin

Tri-locus sequence data reject a Gondwanan origin hypothesis for the African/South Pacific crab genus Hymenosoma

Crabs of the family Hymenosomatidae are common in coastal and shelf regions throughout much of the southern hemisphere. One of the genera in the family, Hymenosoma, is represented in Africa and the South Pacific (Australia and New Zealand). This distribution can be explained either by vicariance (presence of the genus on the Gondwanan supercontinent and divergence following its break-up) or more recent transoceanic dispersal from one region to the other. We tested these hypotheses by reconstructing phylogenetic relationships among the seven presently-accepted species in the genus, as well as examining their placement among other hymenosomatid crabs, using sequence data from two nuclear markers (Adenine Nucleotide Transporter [ANT] exon 2 and 18S rDNA) and three mitochondrial markers (COI, 12S and 16S rDNA). The five southern African representatives of the genus were recovered as a monophyletic lineage, and another southern African species, Neorhynchoplax bovis, was identified as their sister taxon. The two species of Hymenosoma from the South Pacific neither clustered with their African congeners, nor with each other, and should therefore both be placed into different genera. Molecular dating supports a post-Gondwanan origin of the Hymenosomatidae. While long-distance dispersal cannot be ruled out to explain the presence of the family Hymenosomatidae on the former Gondwanan land-masses and beyond, the evolutionary history of the African species of Hymenosoma indicates that a third means of speciation may be important in this group: gradual along-coast dispersal from tropical towards temperate regions, with range expansions into formerly inhospitable habitat during warm climatic phases, followed by adaptation and speciation during subsequent cooler phases

The adaptive potential of subtropical rainbowfish in the face of climate change: heritability and heritable plasticity for the expression of candidate genes

Whilst adaptation and phenotypic plasticity might buffer species against habitat degradation associated with global climate change, few studies making such claims also possess the necessary and sufficient data to support them. Doing so requires demonstration of heritable variation in traits affecting fitness under new environmental conditions. We address this issue using an emerging aquatic system to study adaptation to climate change, the crimson-spotted rainbowfish (Melanotaenia duboulayi), a freshwater species from a region of eastern Australia projected to be affected by marked temperature increases. Captive born M. duboulayi of known pedigree were used to assess the long-term effects of contemporary and 2070-projected summer temperatures on the expression of genes previously identified in a climate change transcriptomics (RNA-Seq) experiment. Nearly all genes responded to increasing temperature. Significant additive genetic variance explained a moderate proportion of transcriptional variation for all genes. Most genes also showed broad-sense genetic variation in transcriptional plasticity. Additionally, molecular pathways of candidate genes co-occur with genes inferred to be under climate-mediated selection in wild M. duboulayi populations. Together, these results indicate the presence of existing variation in important physiological traits, and the potential for adaptive responses to a changing thermal environment.R.J. Scott McCairns, Steve Smith, Minami Sasaki, Louis Bernatchez and Luciano B. Beheregara

Out of the deep: Cryptic speciation in a Neotropical gecko (Squamata, Phyllodactylidae) revealed by species delimitation methods

Levels of biodiversity in the Neotropics are largely underestimated despite centuries of research interest in this region. This is particularly true for the Cerrado, the largest Neotropical savanna and a formally recognized biodiversity hotspot. Molecular species delimitation methods have become essential tools to uncover cryptic species and can be notably robust when coupled with morphological information. We present the first evaluation of the monophyly and cryptic speciation of a widespread Cerrado endemic lizard, Gymnodactylus amarali, using phylogenetic and species-trees methods, as well as a coalescent-based Bayesian species delimitation method. We tested whether lineages resulting from the analyses of molecular data are morphologically diagnosed by traditional meristic scale characters. We recovered eight deeply divergent molecular clades within G. amarali, and two additional ones from seasonally dry tropical forest enclaves between the Cerrado and the Caatinga biomes. Analysis of morphological data statistically corroborated the molecular delimitation for all groups, in a pioneering example of the use of support vector machines to investigate morphological differences in animals. The eight G. amarali clades appear monophyletic and endemic to the Cerrado. They display several different properties used by biologists to delineate species and are therefore considered here as candidates for formal taxonomic description. We also present a preliminary account of the biogeographic history of these lineages in the Cerrado, evidence for speciation of sister lineages in the Cerrado–Caatinga contact, and highlight the need for further morphological and genetic studies to assess cryptic diversity in this biodiversity hotspot.FMCBD was supported by scholarships from ‘Coordenação de Aperfeiçoamento de Pessoal de Nível Superior’ (CAPES) and ‘Conselho Nacional de Desenvolvimento Científico e Tecnológico’ (CNPq). This work was funded by CAPES, CNPq, ‘Fundação de Apoio à Pesquisa do Distrito Federal’ (FAPDF), ‘GENPAC15’ and ‘Rede de Pesquisa Biota do Cerrado’, coordinated by GRC. MTR and JC acknowledge ‘Fundação de Amparo à Pesquisa do Estado de São Paulo’ (FAPESP) for funding and D. Pavan, F. Curcio, M. Dixo, M. Teixeira Jr., N. Silva P. Nunes and, T. Mott for collecting tissues and help in field. LBB thanks additional support provided by the Australian Research Council (ARC DP0556496). We are grateful to Fernanda Werneck for collecting the Gymnodactylus specimens of Manga and Matias Cardoso. We also acknowledge two anonymous reviewers for comments that improved the quality of the manuscript. FMCBD is also grateful to Marina Scalon for commenting on early drafts of the manuscript

Out of the deep: Cryptic speciation in a Neotropical gecko (Squamata, Phyllodactylidae) revealed by species delimitation methods

Levels of biodiversity in the Neotropics are largely underestimated despite centuries of research interest in this region. This is particularly true for the Cerrado, the largest Neotropical savanna and a formally recognized biodiversity hotspot. Molecular species delimitation methods have become essential tools to uncover cryptic species and can be notably robust when coupled with morphological information. We present the first evaluation of the monophyly and cryptic speciation of a widespread Cerrado endemic lizard, Gymnodactylus amarali, using phylogenetic and species-trees methods, as well as a coalescent-based Bayesian species delimitation method. We tested whether lineages resulting from the analyses of molecular data are morphologically diagnosed by traditional meristic scale characters. We recovered eight deeply divergent molecular clades within G. amarali, and two additional ones from seasonally dry tropical forest enclaves between the Cerrado and the Caatinga biomes. Analysis of morphological data statistically corroborated the molecular delimitation for all groups, in a pioneering example of the use of support vector machines to investigate morphological differences in animals. The eight G. amarali clades appear monophyletic and endemic to the Cerrado. They display several different properties used by biologists to delineate species and are therefore considered here as candidates for formal taxonomic description. We also present a preliminary account of the biogeographic history of these lineages in the Cerrado, evidence for speciation of sister lineages in the Cerrado–Caatinga contact, and highlight the need for further morphological and genetic studies to assess cryptic diversity in this biodiversity hotspot.FMCBD was supported by scholarships from ‘Coordenação de Aperfeiçoamento de Pessoal de Nível Superior’ (CAPES) and ‘Conselho Nacional de Desenvolvimento Científico e Tecnológico’ (CNPq). This work was funded by CAPES, CNPq, ‘Fundação de Apoio à Pesquisa do Distrito Federal’ (FAPDF), ‘GENPAC15’ and ‘Rede de Pesquisa Biota do Cerrado’, coordinated by GRC. MTR and JC acknowledge ‘Fundação de Amparo à Pesquisa do Estado de São Paulo’ (FAPESP) for funding and D. Pavan, F. Curcio, M. Dixo, M. Teixeira Jr., N. Silva P. Nunes and, T. Mott for collecting tissues and help in field. LBB thanks additional support provided by the Australian Research Council (ARC DP0556496). We are grateful to Fernanda Werneck for collecting the Gymnodactylus specimens of Manga and Matias Cardoso. We also acknowledge two anonymous reviewers for comments that improved the quality of the manuscript. FMCBD is also grateful to Marina Scalon for commenting on early drafts of the manuscript

Genetic divergence between two phenotypically distinct bottlenose dolphin ecotypes suggests separate evolutionary trajectories

Due to their worldwide distribution and occupancy of different types of environments, bottlenose dolphins display considerable morphological variation. Despite limited understanding about the taxonomic identity of such forms and connectivity among them at global scale, coastal (or inshore) and offshore (or oceanic) ecotypes have been widely recognized in several ocean regions. In the Southwest Atlantic Ocean (SWA), however, there are scarce records of bottlenose dolphins differing in external morphology according to habitat preferences that resemble the coastal‐offshore pattern observed elsewhere. The main aim of this study was to analyze the genetic variability, and test for population structure between coastal (n = 127) and offshore (n = 45) bottlenose dolphins sampled in the SWA to assess whether their external morphological distinction is consistent with genetic differentiation. We used a combination of mtDNA control region sequences and microsatellite genotypes to infer population structure and levels of genetic diversity. Our results from both molecular marker types were congruent and revealed strong levels of structuring (microsatellites FST = 0.385, p < .001; mtDNA FST = 0.183, p < .001; ΦST = 0.385, p < .001) and much lower genetic diversity in the coastal than the offshore ecotype, supporting patterns found in previous studies elsewhere. Despite the opportunity for gene flow in potential “contact zones”, we found minimal current and historical connectivity between ecotypes, suggesting they are following discrete evolutionary trajectories. Based on our molecular findings, which seem to be consistent with morphological differentiations recently described for bottlenose dolphins in our study area, we recommend recognizing the offshore bottlenose dolphin ecotype as an additional Evolutionarily Significant Unit (ESU) in the SWA. Implications of these results for the conservation of bottlenose dolphins in SWA are also discussed

Identification of Genetically Important Individuals of the Rediscovered Floreana Galápagos Giant Tortoise (Chelonoidis elephantopus) Provide Founders for Species Restoration Program

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.Species are being lost at an unprecedented rate due to human-driven environmental changes. The cases in which species declared extinct can be revived are rare. However, here we report that a remote volcano in the Galápagos Islands hosts many giant tortoises with high ancestry from a species previously declared as extinct: Chelonoidis elephantopus or the Floreana tortoise. Of 150 individuals with distinctive morphology sampled from the volcano, genetic analyses revealed that 65 had C. elephantopus ancestry and thirty-two were translocated from the volcano’s slopes to a captive breeding center. A genetically informed captive breeding program now being initiated will, over the next decades, return C. elephantopus tortoises to Floreana Island to serve as engineers of the island’s ecosystems. Ironically, it was the haphazard translocations by mariners killing tortoises for food centuries ago that created the unique opportunity to revive this “lost” species today. CORRECTION PUBLISHED 13 SEPT 2017: The original version of this Article contained an error in the title of the paper, where the word “Provides” was incorrectly given as “Provide”. This has now been corrected in the PDF and HTML versions of the Article and in the accompanying Supplementary Information file. The attached full-text article has been updated to incorporate this change