Elie Poulin

Evolutionary versus ecological success in Antarctic benthic invertebrates

The unusually high proportion of brooding compared with broadcaster species among coastal Antarctic invertebrates has been traditionally interpreted as an adaptation to local environmental conditions. However, species with a planktotrophic developmental mode are ecologically dominant (in terms of abundance of individuals) along Antarctic coastal areas. Therefore, is the apparent ecological success of broadcasters related to their developmental mode? We argue that the present shallow Antarctic benthic invertebrate fauna is the result of two processes acting at different temporal scales. First, the high proportion of brooding species compared with coastal communities elsewhere corresponds to species-level selection occurring over geological and evolutionary times. Second, the ecological dominance of broadcasters is the result of processes operating at ecological timescales that are associated with the advantage of having pelagic larvae under highly disturbed conditions.

WHY ARE THERE SO MANY SPECIES OF BROODING ANTARCTIC ECHINOIDS

Marine invertebrates display a great variety of life‐history traits and reproductive strategies. In echinoids, four patterns of larval development are generally recognized: planktotrophy, pelagic lecithotrophy, bottom dwelling, and brood protecting. Each broad type of free and protected development is found in all the oceans, but comparisons of the principal reproductive modes between different geographic regions have shown that they are not equally distributed. Frequency of pelagic development (planktotrophic and lecithotrophic) decreases from equator to Antarctic, where brood protecting becomes dominant. Numerous theories have been proposed to explain the richness of nonpelagic development in most marine invertebrates within the Southern Ocean. These theories can be grouped into three categories: (1) larval survival, where selection acts on larval; (2) energy allocation; and (3) dispersal. All of them consider the adaptative significance of brood protecting as the key to the success of this strategy in the Antarctic. However, the adaptative significance of brooding and the evolutionary success of this strategy in the Antarctic must be considered as two separate questions. To consider the problem at an evolutionary level, we have examined the consequences of different reproductive strategies on the genetic structure of species and on the long‐term evolution of the clade. We examine this problem in the case of echinoids, a clade particularly well suited to addressing this question. In echinoids, the reduction of larval‐stage duration is associated with a decrease in gene flow and consequently in the geographical scale of genetic differentiation. This allows us to reconsider the high‐speciation‐rate model, which leads to an increase in the number of low‐dispersal species (isolation by distance). This model, previously tested by means of fossils is not satisfactory in living echinoids. Thus, the model is rebuilt with the addition of differential extinction rate between planktotrophic and brooding species in relation with the climatic history of the Antarctic.

Molecular phylogeny and historical biogeography of Nacella (Patellogastropoda: Nacellidae) in the Southern Ocean

The evolution and the historical biogeography of the Southern Ocean marine benthic fauna are closely related to major tectonic and climatic changes that occurred in this region during the last 55 million years (Ma). Several families, genera and even species of marine organisms are shared between distant biogeographic provinces in this region. This pattern of distribution in marine benthic invertebrates has been commonly explained by vicariant speciation due to plate tectonics. However, recent molecular studies have provided new evidence for long-distance dispersion as a plausible explanation of biogeographical patterns in the Southern Ocean. True limpets of the genus Nacella are currently distributed in different biogeographic regions of the Southern Ocean such as Antarctica, Kerguelen Province, southern New Zealand Antipodean Province, North-Central Chile and South American Magellanic Province. Here, we present phylogenetic reconstructions using two mitochondrial DNA markers (Cytochrome Oxidase I and Cytochrome b) to look into the relationships among Nacella species and to determine the origin and diversification of the genus. Phylogenies were reconstructed using two methods, Maximum Parsimony and Bayesian Inference, while divergence time among Nacella species was estimated following a relaxed Bayesian approach. For this purpose, we collected inter- and subtidal species belonging to four biogeographic regions in the Southern Ocean: Antarctica, Kerguelen Province, Central Chile, and Magellanic Province. Our molecular results agree with previous morphological and molecular studies supporting the monophyly of Nacella and its sister relationship with Cellana. Two rounds of diversification are recognized in the evolution of Nacella. The first one occurred at the end of the Miocene and gave rise to the main lineages, currently distributed in Antarctica, South America or Kerguelen Province. Large genetic divergence was detected among Nacella species from these distant biogeographic provinces emphasizing the significance of trans-oceanic discontinuities and suggesting long-distance dispersal was relatively unimportant. The second diversification round consisted of a more recent Pleistocene radiation in the Magellanic region. In this province, different morphological species of Nacella exhibit extreme low levels of genetic divergence with absence of reciprocal monophyly among them. According to our time estimation, the origin and diversification of Nacella in the Southern Ocean is more recent (<15 MY) than the expected under the hypothesis of vicariant speciation due to plate tectonics. The evolution of this genus seems to be closely related to drastic climatic and oceanographic changes in the Southern Ocean during the middle-Miocene climatic transition. In spite of the high number of species described for the Magellanic Province, molecular results indicate that these species are the most derived ones in the evolution of the genus and therefore that the Magellanic region does not need to correspond to the origin center of Nacella. The absence of genetic divergence among these species supports a very recent radiation process accompanied by rapid morphological and ecological diversification.

Phylogeographic Structure in Benthic Marine Invertebrates of the Southeast Pacific Coast of Chile with Differing Dispersal Potential

The role of dispersal potential on phylogeographic structure, evidenced by the degree of genetic structure and the presence of coincident genetic and biogeographic breaks, was evaluated in a macrogeographic comparative approach along the north-central coast of Chile, across the biogeographic transition zone at 30°S. Using 2,217 partial sequences of the mitochondrial Cytochrome Oxidase I gene of eight benthic invertebrate species along ca. 2,600 km of coast, we contrasted dispersal potential with genetic structure and determined the concordance between genetic divergence between biogeographic regions and the biogeographic transition zone at 30°S. Genetic diversity and differentiation highly differed between species with high and low dispersal potential. Dispersal potential, sometimes together with biogeographic region, was the factor that best explained the genetic structure of the eight species. The three low dispersal species, and one species assigned to the high dispersal category, had a phylogeographic discontinuity coincident with the biogeographic transition zone at 30°S. Furthermore, coalescent analyses based on the isolation-with-migration model validate that the split between biogeographic regions north and south of 30°S has a historic origin. The signatures of the historic break in high dispersers is parsimoniously explained by the homogenizing effects of gene flow that have erased the genetic signatures, if ever existed, in high dispersers. Of the four species with structure across the break, only two had significant albeit very low levels of asymmetric migration across the transition zone. Historic processes have led to the current biogeographic and phylogeographic structure of marine species with limited dispersal along the north-central coast of Chile, with a strong lasting impact in their genetic structure.

Ecological and biogeographical inferences on two sympatric and enigmatic Andean cat species using genetic identification of faecal samples

The carnivore community of the altiplano ecosystem of the high Andes, including the Andean mountain cat (Leopardus jacobita) and pampas cat (Leopardus colocolo), is one of the least studied in the world. We determined the origin of 186 carnivore samples (184 faeces and two skulls) collected above 3000 m above sea level in northern Chile, including 33 from the Andean mountain cat and 75 from the pampas cat using diagnostic molecular genetic sequence variation. We determined for the first time food habits, habitat and physiographic associations, and general patterns of molecular genetic variation of the Andean mountain cat and the pampas cat in Chile. Both species had narrow dietary niches dominated by small rodents and there was a wide overlap in diet composition (0.82), suggesting low levels of prey partitioning between species. The mountain viscacha (Lagidium viscacia) made up a large proportion of the biomass of the diet of both species, especially for the Andean mountain cat (93.9% vs. 74.8% for the pampas cat), underscoring the importance of further research and conservation focus on this vanishing prey species. Although the probability of finding Andean mountain cat scats increased with altitude and slope, there was substantial geographical overlap in distribution between species, revealing that the pampas cat distribution includes high‐altitude grassland habitats. The Andean mountain cat had relatively low levels of mitochondrial DNA (mtDNA) genetic variation (two mtDNA haplotypes) compared with the pampas cat (17 mtDNA haplotypes), suggestive of a distinct evolutionary history and relatively smaller historic populations. These insights will facilitate and provide tools and hypotheses for much‐needed research and conservation efforts on these species and this ecosystem.

Concerted genetic, morphological and ecological diversification in Nacella limpets in the Magellanic Province

Common inhabitants of Antarctic and Subantarctic rocky shores, the limpet genus Nacella, includes 15 nominal species distributed in different provinces of the Southern Ocean. The Magellanic Province represents the area with the highest diversity of the genus. Phylogenetic reconstructions showed an absence of reciprocal monophyly and high levels of genetic identity among nominal species in this Province and therefore imply a recent diversification in southern South America. Because most of these taxa coexist along their distribution range with clear differences in their habitat preferences, Nacella is a suitable model to explore diversification mechanisms in an area highly affected by recurrent Pleistocene continental ice cap advances and retreats. Here, we present genetic and morphological comparisons among sympatric Magellanic nominal species of Nacella. We amplified a fragment of the COI gene for 208 individuals belonging to seven sympatric nominal species and performed geometric morphometric analyses of their shells. We detected a complete congruence between genetic and morphological results, leading us to suggest four groups of Nacella among seven analysed nominal species. Congruently, each of these groups was related to different habitat preferences such as bathymetric range and substrate type. A plausible explanation for these results includes an ecologically based allopatric speciation process in Nacella. Major climatic changes during the Plio‐Pleistocene glacial cycles may have enhanced differentiation processes. Finally, our results indicate that the systematics of the group requires a deep revision to re‐evaluate the taxonomy of Nacella and to further understand the Pleistocene legacy of the glacial cycles in the southern tip of South America.

Towards a model of postglacial biogeography in shallow marine species along the Patagonian Province: lessons from the limpet Nacella magellanica (Gmelin, 1791)

BackgroundPatagonia extends for more than 84,000 km of irregular coasts is an area especially apt to evaluate how historic and contemporary processes influence the distribution and connectivity of shallow marine benthic organisms. The true limpet Nacella magellanica has a wide distribution in this province and represents a suitable model to infer the Quaternary glacial legacy on marine benthic organisms. This species inhabits ice-free rocky ecosystems, has a narrow bathymetric range and consequently should have been severely affected by recurrent glacial cycles during the Quaternary. We performed phylogeographic and demographic analyses of N. magellanica from 14 localities along its distribution in Pacific Patagonia, Atlantic Patagonia, and the Falkland/Malvinas Islands.ResultsMitochondrial (COI) DNA analyses of 357 individuals of N. magellanica revealed an absence of genetic differentiation in the species with a single genetic unit along Pacific Patagonia. However, we detected significant genetic differences among three main groups named Pacific Patagonia, Atlantic Patagonia and Falkland/Malvinas Islands. Migration rate estimations indicated asymmetrical gene flow, primarily from Pacific Patagonia to Atlantic Patagonia (Nem=2.21) and the Falkland/Malvinas Islands (Nem=16.6). Demographic reconstruction in Pacific Patagonia suggests a recent recolonization process (< 10 ka) supported by neutrality tests, mismatch distribution and the median-joining haplotype genealogy.ConclusionsAbsence of genetic structure, a single dominant haplotype, lack of correlation between geographic and genetic distance, high estimated migration rates and the signal of recent demographic growth represent a large body of evidence supporting the hypothesis of rapid postglacial expansion in this species in Pacific Patagonia. This expansion could have been sustained by larval dispersal following the main current system in this area. Lower levels of genetic diversity in inland sea areas suggest that fjords and channels represent the areas most recently colonized by the species. Hence recolonization seems to follow a west to east direction to areas that were progressively deglaciated. Significant genetic differences among Pacific, Atlantic and Falkland/Malvinas Islands populations may be also explained through disparities in their respective glaciological and geological histories. The Falkland/Malvinas Islands, more than representing a glacial refugium for the species, seems to constitute a sink area considering the strong asymmetric gene flow detected from Pacific to Atlantic sectors. These results suggest that historical and contemporary processes represent the main factors shaping the modern biogeography of most shallow marine benthic invertebrates inhabiting the Patagonian Province.

Sistemática, taxonomía y domesticación de alpacas y llamas: nueva evidencia cromosómica y molecular

Four camelid species exist in South America: two wild, the guanaco (Lama guanicoe) and the vicuna (Vicugna vicugna), and two domestic, the alpaca (Lama pacos) and the llama (Lama glama). However, the origin of the domestic species has been a matter of debate. In the present study, variations in chromosome G banding patterns and in two mitochondrial gene sequences have been used to study the origin and classification of the llama and alpaca. Similar patterns in chromosome G band structure were observed in all four Lamini species, and these in turn were similar to the bands described for camels, Camelus bactrianus. However, fine and consistent differences were found in the short arms of chromosome 1, separating camels, guanacos and llamas from vicunas and alpacas. This pattern was consistent even in a hybrid guanaco x alpaca. Equivalent relationship

Mitochondrial DNA variation and systematics of the Guanaco (Lama Guanicoe, Artiodactyla: Camelidae)

Abstract Guanacos (Lama guanicoe) are the most important native herbivorous species in the South American steppes and the dominant ungulate in a fauna rich in rodents but poor in large mammal species. Between 2 and 4 subspecies are usually recognized within Lama guanicoe, based on subtle morphological differences and geographic distribution. To evaluate whether molecular variation is consistent with the latter hypotheses, we analyzed the complete cytochrome-b and partial control region mitochondrial DNA sequences of L. guanicoe from 22 localities in Peru, Bolivia, Argentina, and Chile. Sequence analyses of both genes support the monophyly of the species but failed to distinguish the occurrence of subspecies along the geographic range. Despite that, the northernmost populations (Peru and northern Chile) showed some degree of genetic differentiation with respect to southern representatives from Argentina, Bolivia, and rest of Chile. Analysis of genetic diversity also showed a strong signal of past low population size and a recent population expansion.

Extinction and recolonization of maritime Antarctica in the limpet Nacella concinna (Strebel, 1908) during the last glacial cycle: toward a model of Quaternary biogeography in shallow Antarctic invertebrates.

Quaternary glaciations in Antarctica drastically modified geographical ranges and population sizes of marine benthic invertebrates and thus affected the amount and distribution of intraspecific genetic variation. Here, we present new genetic information in the Antarctic limpet Nacella concinna, a dominant Antarctic benthic species along shallow ice‐free rocky ecosystems. We examined the patterns of genetic diversity and structure in this broadcast spawner along maritime Antarctica and from the peri‐Antarctic island of South Georgia. Genetic analyses showed that N. concinna represents a single panmictic unit in maritime Antarctic. Low levels of genetic diversity characterized this population; its median‐joining haplotype network revealed a typical star‐like topology with a short genealogy and a dominant haplotype broadly distributed. As previously reported with nuclear markers, we detected significant genetic differentiation between South Georgia Island and maritime Antarctica populations. Higher levels of genetic diversity, a more expanded genealogy and the presence of more private haplotypes support the hypothesis of glacial persistence in this peri‐Antarctic island. Bayesian Skyline plot and mismatch distribution analyses recognized an older demographic history in South Georgia. Approximate Bayesian computations did not support the persistence of N. concinna along maritime Antarctica during the last glacial period, but indicated the resilience of the species in peri‐Antarctic refugia (South Georgia Island). We proposed a model of Quaternary Biogeography for Antarctic marine benthic invertebrates with shallow and narrow bathymetric ranges including (i) extinction of maritime Antarctic populations during glacial periods; (ii) persistence of populations in peri‐Antarctic refugia; and (iii) recolonization of maritime Antarctica following the deglaciation process.