Marcelo Vallinoto

Realized niche shift during a global biological invasion.

Significance Species’ distributions result from dispersal and physiological constraints, interactions with other species, and ultimately, evolution. Biological invasions result from the deliberate or accidental movement of species between regions they would not reach through natural dispersal and can cause major conservation, economic, and human health issues. However, invasions also provide fascinating insights into species’ distribution limits. We investigate the invasion of the cane toad from South America to Australia by comparing the results of two modeling approaches: one considering physiological constraints and the other considering the joint influences of physiology, dispersal, and biotic interactions. Our findings demonstrate that the cane toad is limited in its native distribution by biotic interactions but, in Australia, is free to fill its climatic potential. Accurate forecasts of biological invasions are crucial for managing invasion risk but are hampered by niche shifts resulting from evolved environmental tolerances (fundamental niche shifts) or the presence of novel biotic and abiotic conditions in the invaded range (realized niche shifts). Distinguishing between these kinds of niche shifts is impossible with traditional, correlative approaches to invasion forecasts, which exclusively consider the realized niche. Here we overcome this challenge by combining a physiologically mechanistic model of the fundamental niche with correlative models based on the realized niche to study the global invasion of the cane toad Rhinella marina. We find strong evidence that the success of R. marina in Australia reflects a shift in the species’ realized niche, as opposed to evolutionary shifts in range-limiting traits. Our results demonstrate that R. marina does not fill its fundamental niche in its native South American range and that areas of niche unfilling coincide with the presence of a closely related species with which R. marina hybridizes. Conversely, in Australia, where coevolved taxa are absent, R. marina largely fills its fundamental niche in areas behind the invasion front. The general approach taken here of contrasting fundamental and realized niche models provides key insights into the role of biotic interactions in shaping range limits and can inform effective management strategies not only for invasive species but also for assisted colonization under climate change.

Analysis of mitochondrial D-loop region casts new light on domestic water buffalo (Bubalus bubalis) phylogeny

The phylogeny of water buffaloes (Bubalus bubalis) is still a matter of discussion, especially if the two types of domestic water buffalo (swamp and river) derived from different domestication events or if they are products of human selection. To obtain more insight, we analyzed the entire mitochondrial D-loop region of 80 water buffaloes of four different breeds, i.e., 19 swamp buffaloes (Carabao) and 61 river buffaloes (Murrah, Jafarabadi, and Mediterranean), sampled in Brazil and Italy. We detected 36 mitochondrial haplotypes with 128 polymorphic sites. Pooled with published data of South-East Asian and Australian water buffaloes and based on comprehensive median-joining network and population demography analyses we show evidence that both river and swamp buffaloes decent from one domestication event, probably in the Indian subcontinent. However, the today swamp buffaloes have an unravelled mitochondrial history, which can be explained by introgression of wild water buffalo mtDNA into domestic stocks. We are also discussing indications for an independent domestication of buffaloes in China.

New primers for the amplification and sequencing of nuclear loci in a taxonomically wide set of reptiles and amphibians

We report new primers for the amplification and sequencing of 11 nuclear markers in squamate reptiles and anuran amphibians (five in squamates, six in anurans). Ten out of the 11 loci are introns (three of which are linked) that were amplified using an exon-primed, intron-crossing (EPIC) PCR strategy, whereas an eleventh locus spans part of a protein-coding gene. Squamate and anuran primers were initially developed for Lacerta schreiberi (Squamata: Lacertidae) and Pelodytes spp. (Anura: Pelodytidae), respectively. Cross-species amplification of the squamate markers was evaluated in four genera representing two additional families, whereas for anurans three genera corresponding to three additional families were tested. Three out of the five loci were successfully sequenced in all squamate taxa tested. Cross-amplification of the six anuran markers had lower, but still significant, success. We predict these markers will be of great utility for both population genetics and phylogenetic studies.

Hybridization and massive mtDNA unidirectional introgression between the closely related Neotropical toads Rhinella marina and R. schneideri inferred from mtDNA and nuclear markers

BackgroundThe classical perspective that interspecific hybridization in animals is rare has been changing due to a growing list of empirical examples showing the occurrence of gene flow between closely related species. Using sequence data from cyt b mitochondrial gene and three intron nuclear genes (RPL9, c-myc, and RPL3) we investigated patterns of nucleotide polymorphism and divergence between two closely related toad species R. marina and R. schneideri. By comparing levels of differentiation at nuclear and mtDNA levels we were able to describe patterns of introgression and infer the history of hybridization between these species.ResultsAll nuclear loci are essentially concordant in revealing two well differentiated groups of haplotypes, corresponding to the morphologically-defined species R. marina and R. schneideri. Mitochondrial DNA analysis also revealed two well-differentiated groups of haplotypes but, in stark contrast with the nuclear genealogies, all R. schneideri sequences are clustered with sequences of R. marina from the right Amazon bank (RAB), while R. marina sequences from the left Amazon bank (LAB) are monophyletic. An Isolation-with-Migration (IM) analysis using nuclear data showed that R. marina and R. schneideri diverged at ≈ 1.69 Myr (early Pleistocene), while R. marina populations from LAB and RAB diverged at ≈ 0.33 Myr (middle Pleistocene). This time of divergence is not consistent with the split between LAB and RAB populations obtained with mtDNA data (≈ 1.59 Myr), which is notably similar to the estimate obtained with nuclear genes between R. marina and R. schneideri. Coalescent simulations of mtDNA phylogeny under the speciation history inferred from nuclear genes rejected the hypothesis of incomplete lineage sorting to explain the conflicting signal between mtDNA and nuclear-based phylogenies.ConclusionsThe cytonuclear discordance seems to reflect the occurrence of interspecific hybridization between these two closely related toad species. Overall, our results suggest a phenomenon of extensive mtDNA unidirectional introgression from the previously occurring R. schneideri into the invading R. marina. We hypothesize that climatic-induced range shifts during the Pleistocene/Holocene may have played an important role in the observed patterns of introgression.

A molecular analysis of the evolutionary relationships in the Callitrichinae, with emphasis on the position of the dwarf marmoset

Schneider, H., Bernardi, J. A. R., da Cunha, D. B., Tagliaro, C. H., Vallinoto, M., Ferrari, S. F. & Sampaio, I. (2011). A molecular analysis of the evolutionary relationships in the Callitrichinae, with emphasis on the position of the dwarf marmoset. —Zoologica Scripta, 41, 1–10.

Phylogeny and biogeography of the Rhinella marina species complex (Amphibia, Bufonidae) revisited: implications for Neotropical diversification hypotheses

Vallinoto, M., Sequeira, F., Sodré, D., Bernardi, J. A. R., Sampaio, I. & Schneider, H. (2009). Phylogeny and biogeography of the Rhinella marina species complex (Amphibia, Bufonidae) revisited: implications for Neotropical diversification hypotheses. —Zoologica Scripta, 39, 128–140.

Mitochondrial COII gene sequences provide new insights into the phylogeny of marmoset species groups (Callitrichidae, Primates).

Mitochondrial cytochrome oxidase II (COII) gene sequences (549 base pairs) were used to investigate the taxonomic relationships among 12 marmoset (Callithrix, Cebuella and Mico) taxa. A large number of substitutions were found in the third base codon positions, providing a strong phylogenetic signal in a gene coding a conserved protein. Despite the significant affinity between the 2 Amazonian genera Cebuella and Mico, found in recent molecular studies, the analysis presented here did not resolve convincingly the phylogenetic relationships between the 3 genera. Mico nevertheless formed 3 distinct clades, reflecting a basic division of species groups based on geographic distribution (east or west of the Rio Tapajós) rather than morphology (presence or absence of auricular hair). This supports the taxonomic distinction of the allopatric emiliae forms. In Callithrix, Callithrix aurita forms a distinct clade, but the remaining morphotypes form a somewhat contradictory cluster, possibly resulting from an extremely rapid radiation.

Low levels of genetic diversity depicted from mitochondrial DNA sequences in a heavily exploited marine fish (Cynoscion acoupa, Sciaenidae) from the Northern coast of Brazil

The acoupa weakfish (Cynoscion acoupa - Sciaenidae) is a marine species of croaker with estuarine-dependent behavior, found in the western Atlantic from Panama to Argentina. It is one of the most exploited food fish on the northern coast of Brazil. In this study, DNA sequences were determined from the entire control region (D-loop) of the mitochondrial genome of 297 individuals collected during seven different months between December 2003 and August 2005 on the northern coast of Brazil (Amapa and Para). Genetic variability expressed by haplotype (h = 0,892) and nucleotide (p = 0,003) diversities were low compared to other heavily exploited marine fish species from the western Atlantic and eastern Asia. AMOVA depicted a lack of genetic structuring among the samples from different years, indicating the presence of a single stock of C. acoupa within the sample area. The possible reasons for the low levels of genetic diversity are discussed. These results demonstrate a need for the monitoring of C. acoupa harvesting and the preservation of the estuaries within its geographic range, considering that this large fish depends on estuarine ecosystems during part of its life cycle.

Tocantins river as an effective barrier to gene flow in Saguinus niger populations

The Saguinus represent the basal genus of the Callitrichinae subfamily. Traditionally this genus is divided into three groups: Hairy, Mottled and Bare-face, however, molecular data failed to validate these groups as monophyletic units, as well as raised some subspecies to the species status. This is the case of the former subspecies Saguinus midas midas and S. midas niger, which are now considered as different species. In the present study, we sequenced a portion of the D-loop mtDNA region in populations from the East bank of the Xingu and from both banks of the Tocantins river, in order to test the effectiveness of large rivers as barriers to the gene flow in Saguinus. According to our results, the populations from the East and West banks of the Tocantins river are more divergent than true species like S. mystax and S. imperator. The Tocantins river may be acting as a barrier to gene flow, and consequently these very divergent populations may represent distinct taxonomic entities (species?).

Can Lutjanus purpureus (South red snapper) be "legally" considered a red snapper (Lutjanus campechanus)?

Red snappers (Lutjanus purpureus in Brazil and Lutjanus campechanus in USA and Gulf of Mexico) are both under clear effect of overfishing. Because of their high morphological similarity it has already been suggested that they could possibly be considered as a single species. To investigate the degree of similarity and the genetic structure of red snapper populations we constructed a common dataset of partial D-loop mtDNA sequences of L. purpureus from Brazil (Amapa, Para and Maranhao) and L. campechanus from the Atlantic coast of the USA (Florida, Louisiana and Mississippi). Phylogenetic and population genetic analyses surprisingly depicted high similarity between L. campechanus and L. purpureus, compatible with the hypothesis of a single species of red snapper for the Western Atlantic Ocean. These preliminary but very curious findings open an important discussion regarding the legislation involved on the capture of this overexploited fish resources as well as regarding their taxonomy.