Publications by authors named "Stephen C Lougheed"

49 Publications

Depth-Dependent Spatiotemporal Dynamics of Overwintering Pelagic in a Temperate Water Body.

Microorganisms 2021 Aug 12;9(8). Epub 2021 Aug 12.

Department of Biology, Queen's University, Kingston, ON K7L 3N6, Canada.

Cyanobacteria in the genus are dominant components of many harmful algal blooms worldwide. Their pelagic-benthic life cycle helps them survive periods of adverse conditions and contributes greatly to their ecological success. Many studies on overwintering have focused on benthic colonies and suggest that sediment serves as the major inoculum for subsequent summer blooms. However, the contemporaneous overwintering pelagic population may be important as well but is understudied. In this study, we investigated near-surface and near-bottom pelagic population dynamics of both microcystin-producing and total over six weeks in winter at Dog Lake (South Frontenac, ON, Canada). We quantified relative concentrations using real-time PCR. Our results showed that the spatiotemporal distribution of overwintering pelagic was depth dependent. The abundance of near-bottom pelagic declined with increased depth with no influence of depth on near-surface abundance. In the shallow region of the lake (<10 m), most pelagic was found near the lake bottom (>90%). However, the proportion of near-surface rose sharply to over 60% as the depth increased to approximately 18 m. The depth-dependent distribution pattern was found to be similar in both microcystin-producing and total Our results suggest the top of the water column may be a more significant contributor of recruitment inoculum than previously thought and merits more attention in early CHAB characterization and remediation.
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http://dx.doi.org/10.3390/microorganisms9081718DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8399979PMC
August 2021

Cytonuclear discordance in the crowned-sparrows, Zonotrichia atricapilla and Zonotrichia leucophrys.

Mol Phylogenet Evol 2021 09 1;162:107216. Epub 2021 Jun 1.

Department of Biology, Queen's University, Kingston, ON K7L 3N6, Canada. Electronic address:

The golden-crowned (Zonotrichia atricapilla) and white-crowned (Z. leucophrys) sparrows have been presented as a compelling case for rapid speciation. They display divergence in song and plumage with overlap in their breeding ranges implying reproductive isolation, but have almost identical mitochondrial genomes. Previous research proposed hybridization and subsequent mitochondrial introgression as an alternate explanation, but lacked robust nuclear gene trees to distinguish between introgression and incomplete lineage sorting. We test for signatures of these processes between Z. atricapilla and Z. leucophrys, and investigate the relationships among Z. leucophrys subspecies, using mitochondrial sequencing and a reduced representation nuclear genomic dataset. Contrary to the paraphyly evident in mitochondrial gene trees, we confirmed the reciprocal monophyly of Z. atricapilla and Z. leucophrys using large panels of single nucleotide polymorphisms (SNPs). The pattern of cytonuclear discordance is consistent with limited, historical hybridization and mitochondrial introgression, rather than a recent origin and incomplete lineage sorting between recent sister species. We found evidence of nuclear phylogeographic structure within Z. leucophrys with two distinct clades. Altogether, our results indicate deeper divergences between Z. atricapilla and Z. leucophrys than inferred using mitochondrial markers. Our results demonstrate the limitations of relying solely on mitochondrial DNA for taxonomy, and raise questions about the possibility of selection on the mitochondrial genome during temperature oscillations (e.g. during the Pleistocene). Historical mitochondrial introgression facilitated by past environmental changes could cause erroneous dating of lineage splitting in other taxa when based on mitochondrial DNA alone.
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http://dx.doi.org/10.1016/j.ympev.2021.107216DOI Listing
September 2021

Identification of Arctic Food Fish Species for Anthropogenic Contaminant Testing Using Geography and Genetics.

Foods 2020 Dec 8;9(12). Epub 2020 Dec 8.

Department of Biology, Queen's University, Kingston, ON K7L 3N6, Canada.

The identification of food fish bearing anthropogenic contaminants is one of many priorities for Indigenous peoples living in the Arctic. Mercury (Hg), arsenic (As), and persistent organic pollutants including polychlorinated biphenyls (PCBs) are of concern, and these are reported, in some cases for the first time, for fish sampled in and around King William Island, located in Nunavut, Canada. More than 500 salmonids, comprising Arctic char, lake trout, lake whitefish, and ciscoes, were assayed for contaminants. The studied species are anadromous, migrating to the ocean to feed in the summers and returning to freshwater before sea ice formation in the autumn. Assessments of muscle Hg levels in salmonids from fishing sites on King William Island showed generally higher levels than from mainland sites, with mean concentrations generally below guidelines, except for lake trout. In contrast, mainland fish showed higher means for As, including non-toxic arsenobetaine, than island fish. Lake trout were highest in As and PCB levels, with salmonid PCB congener analysis showing signatures consistent with the legacy of cold-war distant early warning stations. After DNA-profiling, only 4-32 Arctic char single nucleotide polymorphisms were needed for successful population assignment. These results support our objective to demonstrate that genomic tools could facilitate efficient and cost-effective cluster assignment for contaminant analysis during ocean residency. We further suggest that routine pollutant testing during the current period of dramatic climate change would be helpful to safeguard the wellbeing of Inuit who depend on these fish as a staple input to their diet. Moreover, this strategy should be applicable elsewhere.
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http://dx.doi.org/10.3390/foods9121824DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7764770PMC
December 2020

Comparing fish prey diversity for a critically endangered aquatic mammal in a reserve and the wild using eDNA metabarcoding.

Sci Rep 2020 10 7;10(1):16715. Epub 2020 Oct 7.

Department of Biology, Queen's University, Kingston, ON, Canada.

Using environmental DNA (eDNA) metabarcoding, we compared fish diversity in two distinct water bodies within the Yangtze River Basin with known populations of the critically endangered Yangtze finless porpoise (Neophocaena asiaeorientalis; YFP): the Tian-e-Zhou Reserve and Poyang Lake. We aimed to create a fish surveying tool for use in the Yangtze River Basin, while also gaining a better understanding of the prey distribution and diversity within two of the remaining strongholds of YFP. 16S rRNA universal primers were developed to amplify fish eDNA. After high-throughput sequencing and stringent data filtering, we identified a total of 75 fish species (6 orders, 9 families, 57 genera) across seasons and regions. Nine of the 75 fish species were among the 28 known YFP prey species, three of which were detected in all water samples. Our eDNA metabarcoding identified many species that had been previously captured using traditional netting practices, but also numerous species not previously collected in these water bodies. Fish diversity was higher in Poyang Lake than in Tian-e-Zhou Reserve, as well as higher in the spring than in summer. These methods provide a broadly applicable tool to quantify fish diversity and distributions throughout the Yangtze River Basin, and to inform conservation strategies of YFP.
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http://dx.doi.org/10.1038/s41598-020-73648-2DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7542144PMC
October 2020

Canadian polar bear population structure using genome-wide markers.

Ecol Evol 2020 Apr 24;10(8):3706-3714. Epub 2020 Mar 24.

Department of Biology Queen's University Kingston ON Canada.

Predicting the consequences of environmental changes, including human-mediated climate change on species, requires that we quantify range-wide patterns of genetic diversity and identify the ecological, environmental, and historical factors that have contributed to it. Here, we generate baseline data on polar bear population structure across most Canadian subpopulations ( = 358) using 13,488 genome-wide single nucleotide polymorphisms (SNPs) identified with double-digest restriction site-associated DNA sequencing (ddRAD). Our ddRAD dataset showed three genetic clusters in the sampled Canadian range, congruent with previous studies based on microsatellites across the same regions; however, due to a lack of sampling in Norwegian Bay, we were unable to confirm the existence of a unique cluster in that subpopulation. These data on the genetic structure of polar bears using SNPs provide a detailed baseline against which future shifts in population structure can be assessed, and opportunities to develop new noninvasive tools for monitoring polar bears across their range.
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http://dx.doi.org/10.1002/ece3.6159DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7160183PMC
April 2020

A real-time PCR assay to accurately quantify polar bear DNA in fecal extracts.

PeerJ 2020 7;8:e8884. Epub 2020 Apr 7.

Department of Biology, Queen's University, Kingston, ON, Canada.

DNA extracted from fecal samples contains DNA from the focal species, food, bacteria and pathogens. Most DNA quantification methods measure total DNA and cannot differentiate among sources. Despite the desirability of noninvasive fecal sampling for studying wildlife populations, low amounts of focal species DNA make it difficult to use for next-generation sequencing (NGS), where accurate DNA quantification is critical for normalization. Two factors are required prior to using fecal samples in NGS libraries: (1) an accurate quantification method for the amount of target DNA and (2) a determination of the relative amount of target DNA needed for successful single nucleotide polymorphism genotyping assays. Here, we address these needs by developing primers to amplify a 101 bp region of the nuclear gene and a quantitative PCR (qPCR) assay that allows the accurate quantification of the amount of polar bear () DNA in fecal extracts. We test the assay on pure polar bear DNA extracted from muscle tissue and find a high correlation between fluorometric and qPCR quantifications. The qPCR assay was also successfully used to quantify the amount of DNA derived from polar bears in fecal extractions. Orthologs of the gene have been identified across vertebrates; thus, similar qPCR assays could be developed for other species to enable noninvasive studies.
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http://dx.doi.org/10.7717/peerj.8884DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7147431PMC
April 2020

Food quality effects on instar-specific life histories of a holometabolous insect.

Ecol Evol 2020 Jan 3;10(2):626-637. Epub 2020 Jan 3.

Department of Biology Queen's University Kingston ON Canada.

It is a long-standing challenge to understand how changes in food resources impact consumer life history traits and, in turn, impact how organisms interact with their environment. To characterize food quality effects on life history, most studies follow organisms throughout their life cycle and quantify major life events, such as age at maturity or fecundity. From these studies, we know that food quality generally impacts body size, juvenile development, and life span. Importantly, throughout juvenile development, many organisms develop through several stages of growth that can have different interactions with their environment. For example, some parasitoids typically attack larger instars, whereas larval insect predators typically attack smaller instars. Interestingly, most studies lump all juvenile stages together, which ignores these ecological changes over juvenile development.We combine a cross-sectional experimental approach with a stage-structured population model to estimate instar-specific vital rates in the bean weevil, across a food quality gradient. We characterize food quality effects on the bean weevil's life history traits throughout its juvenile ontogeny to test how food quality impacts instar-specific vital rates.Vital rates differed across food quality treatments within each instar; however, their effect differed with instar. Weevils consuming low-quality food spent 38%, 37%, and 18% more time, and were 34%, 53%, and 63% smaller than weevils consuming high-quality food in the second, third, and fourth instars, respectively. Overall, our results show that consuming poor food quality means slower growth, but that food quality effects on vital rates, growth and development are not equal across instars. Differences in life history traits over juvenile ontogeny in response to food quality may impact how organisms interact with their environment, including how susceptible they are to predation, parasitism, and their competitive ability.
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http://dx.doi.org/10.1002/ece3.5790DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6988550PMC
January 2020

Cryptic species and independent origins of allochronic populations within a seabird species complex (Hydrobates spp.).

Mol Phylogenet Evol 2019 10 3;139:106552. Epub 2019 Jul 3.

Department of Biology, Queen's University, Kingston, Ontario, Canada.

Humans are inherently biased towards naming species based on morphological differences, which can lead to reproductively isolated species being mistakenly classified as one if they are morphologically similar. Recognising cryptic diversity is needed to understand drivers of speciation fully, and for accurate estimates of global biodiversity and assessments for conservation. We investigated cryptic species across the range of band-rumped storm-petrels (Hydrobates spp.): highly pelagic, nocturnal seabirds that breed on tropical and sub-tropical islands in the Atlantic and Pacific Oceans. In many breeding colonies, band-rumped storm-petrels have sympatric but temporally isolated (allochronic) populations; we sampled all breeding locations and allochronic populations. Using mitochondrial control region sequences from 754 birds, cytochrome b sequences from 69 birds, and reduced representation sequencing of the nuclear genomes of 133 birds, we uncovered high levels of genetic structuring. Population genomic analyses revealed up to seven unique clusters, and phylogenomic reconstruction showed that these represent seven monophyletic groups. We uncovered up to six independent breeding season switches across the phylogeny, spanning the continuum from genetically undifferentiated temporal populations to full allochronic species. Thus, band-rumped storm-petrels encompass multiple cryptic species, with non-geographic barriers potentially comprising strong barriers to gene flow.
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http://dx.doi.org/10.1016/j.ympev.2019.106552DOI Listing
October 2019

Spatial distribution, prevalence and diversity of haemosporidians in the rufous-collared sparrow, Zonotrichia capensis.

Parasit Vectors 2019 Jan 3;12(1). Epub 2019 Jan 3.

Departamento de Ecosistemas y Medio Ambiente, Facultad de Agronomía e Ingeniería Forestal, Pontificia Universidad Católica de Chile, Código Postal: 6904411, Casilla 306, Correo, 22, Santiago, Chile.

Background: Parasite prevalence and diversity are determined by the distribution of hosts and vectors and by the interplay among a suite of environmental factors. Distributions of parasite lineages vary based on host susceptibility and geographical barriers. Hemoparasites of the genera Haemoproteus and Plasmodium have wide distributions, and high prevalence and genetic diversity within perching birds (Order Passeriformes). The rufous-collared sparrow (Zonotrichia capensis) is widely distributed in Central and South America across an immense diversity of environments from sea level to more than 4000 meters above sea level. It therefore provides an excellent model to investigate whether altitudinal and latitudinal gradients influence the distribution, prevalence and diversity of haemosporidian parasites, their population structure and the biogeographical boundaries of distinct parasite lineages.

Results: We assembled samples from 1317 rufous-collared sparrows spanning 75 locales from across Central and South America (between 9.5°N and 54°S; 10-4655 meters above sea level). We used DNA sequence data from a fragment of the mitochondrial cytochrome b gene (cytb) of Haemoproteus and Plasmodium from 325 positive samples and found prevalences of 22 and 3%, respectively. Haemoproteus exhibited a higher prevalence than Plasmodium but with comparatively lower genetic diversity. We detected a relationship of Plasmodium and Haemoproteus prevalence with altitude and latitude; however, altitude and latitude did not influence parasite diversity.

Conclusions: Parasite lineages showed a phylogeographical boundary coincident with the Andes Mountains, although we also observed a north-south disjunction in Peru for Haemoproteus. Haemosporidian distribution was not homogeneous but differed based on latitude and altitude. This is most probably due to environmental factors that have influenced both vector distribution and abundance, as well as parasite development. Our study provides key insights on the distribution of haemoparasite lineages and parasite dynamics within hosts.
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http://dx.doi.org/10.1186/s13071-018-3243-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6318949PMC
January 2019

Migratory connectivity in the Loggerhead Shrike ().

Ecol Evol 2018 Nov 24;8(22):10662-10672. Epub 2018 Oct 24.

Department of Biology Queen's University Kingston Ontario.

Aim: We combine genetic and stable isotope data to quantify migration patterns in Loggerhead Shrike (), a species of conservation concern in North America, to assess how connectivity differs and impacts population evolution, ecology, and conservation.

Location: We sampled shrikes across the majority of their nonbreeding range, from the Atlantic Coast to the western United States east of the Rocky Mountains and throughout Mexico.

Methods: Our study used a Bayesian framework using δH from a breeding season origin feather and nuclear genetic microsatellite markers to distinguish between co-occurring migratory and nonmigratory individuals on the wintering grounds and, for migrants, to assign individuals to a breeding ground origin and genetic group.

Results: Migratory shrikes were present throughout the nonbreeding range but the proportion differed among sample areas. Four main wintering areas were identified. Connectivity ranged from weakly negative in birds wintering on the Atlantic Coast to strongly positive between wintering grounds in the southwestern United States and Mexico and northwestern breeding populations. Connectivity was weakest in , and strongest in and . Although believed to be nonmigratory, long-distance movements of individuals were observed in and . Our data support a pattern of chain migration, again most notable in the western half of the species nonbreeding range, and differential migration based on age.

Main Conclusions: Our study provides of one such of the first quantitative measures of migratory connectivity and is among the first studies of a short-distance migratory passerine in North America. The higher migratory connectivity among western, versus eastern populations, and less severe population declines attributable to habitat loss or reproductive success, may result in more localized and/or less severe limiting factors for western populations and more severe on the Atlantic coast and Mississippi Alluvial Valley wintering grounds.
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http://dx.doi.org/10.1002/ece3.4415DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6262747PMC
November 2018

Response to climate change of montane herbaceous plants in the genus Rhodiola predicted by ecological niche modelling.

Sci Rep 2018 04 12;8(1):5879. Epub 2018 Apr 12.

The Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, Institute of Biodiversity Science, Institute of Botany, Fudan University, Shanghai, 200438, China.

Climate change profoundly influences species distributions. These effects are evident in poleward latitudinal range shifts for many taxa, and upward altitudinal range shifts for alpine species, that resulted from increased annual global temperatures since the Last Glacial Maximum (LGM, ca. 22,000 BP). For the latter, the ultimate consequence of upward shifts may be extinction as species in the highest alpine ecosystems can migrate no further, a phenomenon often characterized as "nowhere to go". To predict responses to climate change of the alpine plants on the Qinghai-Tibetan Plateau (QTP), we used ecological niche modelling (ENM) to estimate the range shifts of 14 Rhodiola species, beginning with the Last Interglacial (ca. 120,000-140,000 BP) through to 2050. Distributions of Rhodiola species appear to be shaped by temperature-related variables. The southeastern QTP, and especially the Hengduan Mountains, were the origin and center of distribution for Rhodiola, and also served as refugia during the LGM. Under future climate scenario in 2050, Rhodiola species might have to migrate upward and northward, but many species would expand their ranges contra the prediction of the "nowhere to go" hypothesis, caused by the appearance of additional potential habitat concomitant with the reduction of permafrost with climate warming.
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http://dx.doi.org/10.1038/s41598-018-24360-9DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5897335PMC
April 2018

Phytogeographic patterns and cryptic diversity in an aposematic toad from NW Argentina.

Mol Phylogenet Evol 2017 11 24;116:248-256. Epub 2017 Jul 24.

Department of Biology, Queen's University, Kingston, Ontario K7L 3N6, Canada. Electronic address:

The Yungas Redbelly Toad, Melanophryniscus rubriventris, is patchily distributed in Argentina, confined to the upland portion (1000-2000m above sea level) of the montane forests of northern and central regions of Salta, and in central-eastern and south-eastern Jujuy. This species is known for its striking aposematic color variation across its geographic distribution, and was once treated as a complex of three subspecies based on distinctive color patterns. Here we assess the geographical genetic variation within M. rubriventris and quantify divergence in color and pattern among individuals sampled from Northwestern Argentina. We compare multi-gene phylogeography of M. rubriventris to patterns of dorsal and ventral coloration to test whether evolutionary affinities predict variation in warning color. Our results reveal two well-supported species lineages: one confined to the extreme northern portion of our sampling area, and the other extending over most of the Argentine portion of the species' range, within which there are two populations. However, these well-supported evolutionary relationships do not mirror the marked variation in warning coloration. This discordance between DNA genealogy and warning color variation may reflect selection brought about by differences in local predation pressures, potentially coupled with effects of sexual selection and thermoregulation.
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http://dx.doi.org/10.1016/j.ympev.2017.07.013DOI Listing
November 2017

Developing approaches for linear mixed modeling in landscape genetics through landscape-directed dispersal simulations.

Ecol Evol 2017 06 18;7(11):3751-3761. Epub 2017 Apr 18.

School of Environment, Resources and Sustainability University of Waterloo Waterloo ON Canada.

Dispersal can impact population dynamics and geographic variation, and thus, genetic approaches that can establish which landscape factors influence population connectivity have ecological and evolutionary importance. Mixed models that account for the error structure of pairwise datasets are increasingly used to compare models relating genetic differentiation to pairwise measures of landscape resistance. A model selection framework based on information criteria metrics or explained variance may help disentangle the ecological and landscape factors influencing genetic structure, yet there are currently no consensus for the best protocols. Here, we develop landscape-directed simulations and test a series of replicates that emulate independent empirical datasets of two species with different life history characteristics (greater sage-grouse; eastern foxsnake). We determined that in our simulated scenarios, AIC and BIC were the best model selection indices and that marginal values were biased toward more complex models. The model coefficients for landscape variables generally reflected the underlying dispersal model with confidence intervals that did not overlap with zero across the entire model set. When we controlled for geographic distance, variables not in the underlying dispersal models (i.e., nontrue) typically overlapped zero. Our study helps establish methods for using linear mixed models to identify the features underlying patterns of dispersal across a variety of landscapes.
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http://dx.doi.org/10.1002/ece3.2825DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5468135PMC
June 2017

Systematics of the Dendropsophus leucophyllatus species complex (Anura: Hylidae): Cryptic diversity and the description of two new species.

PLoS One 2017 1;12(3):e0171785. Epub 2017 Mar 1.

Museo de Zoología, Escuela de Biología, Pontificia Universidad Católica del Ecuador, Quito, Ecuador.

Genetic data in studies of systematics of Amazonian amphibians frequently reveal that purportedly widespread single species in reality comprise species complexes. This means that real species richness may be significantly higher than current estimates. Here we combine genetic, morphological, and bioacoustic data to assess the phylogenetic relationships and species boundaries of two Amazonian species of the Dendropsophus leucophyllatus species group: D. leucophyllatus and D. triangulum. Our results uncovered the existence of five confirmed and four unconfirmed candidate species. Among the confirmed candidate species, three have available names: Dendropsophus leucophyllatus, Dendropsophus triangulum, and Dendropsophus reticulatus, this last being removed from the synonymy of D. triangulum. A neotype of D. leucophyllatus is designated. We describe the remaining two confirmed candidate species, one from Bolivia and another from Peru. All confirmed candidate species are morphologically distinct and have much smaller geographic ranges than those previously reported for D. leucophyllatus and D. triangulum sensu lato. Dendropsophus leucophyllatus sensu stricto occurs in the Guianan region. Dendropsophus reticulatus comb. nov. corresponds to populations in the Amazon basin of Brazil, Ecuador, and Peru previously referred to as D. triangulum. Dendropsophus triangulum sensu stricto is the most widely distributed species; it occurs in Amazonian Ecuador, Peru and Brazil, reaching the state of Pará. We provide accounts for all described species including an assessment of their conservation status.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0171785PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5332023PMC
August 2017

Closely related species of birds differ more in body size when their ranges overlap--in warm, but not cool, climates.

Evolution 2015 07 14;69(7):1701-12. Epub 2015 Jul 14.

Department of Biology, Queen's University, Kingston, Ontario, Canada, K7L 3N6.

Differences in body size are widely thought to allow closely related species to coexist in sympatry, but body size also varies as an adaptive response to climate. Here, we use a sister lineage approach to test the prediction that body size differences between closely related species of birds worldwide are greater for species whose ranges are sympatric rather than allopatric. We further test if body size differences among sympatric versus allopatric species vary with geography, evolutionary distance, and environmental temperatures. We find greater differences in size among sympatric compared with allopatric lineages, but only in closely related species that live where mean annual temperatures are above 25°C. These size differences in warm environments declined with the evolutionary distance between sister lineages. In species living in cooler regions, closely related allopatric and sympatric species did not differ significantly in size, suggesting either that colder temperatures constrain the evolutionary divergence of size in sympatry, or that the biotic selective pressures favoring size differences in sympatry are weaker in colder environments. Our results are consistent with suggestions by Wallace, Darwin, and Dobzhansky that climatic selective pressures are more important in cooler environments (e.g., high elevations and latitudes) whereas biotic selective pressures dominate in warm environments (e.g., lowland tropics).
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http://dx.doi.org/10.1111/evo.12706DOI Listing
July 2015

Color patterns of closely related bird species are more divergent at intermediate levels of breeding-range sympatry.

Am Nat 2015 Apr 17;185(4):443-51. Epub 2015 Feb 17.

Department of Biology, Queen's University, Kingston, Ontario K7L 3N6, Canada.

Closely related species of birds often differ markedly in their color patterns. Here we examine the influence of breeding-range overlap (breeding sympatry) on the evolution of color pattern differences in a sample of closely related bird species. We used a sister-lineage method to analyze 73 phylogenetically independent comparisons among 246 species and 39 families of birds worldwide. We found that divergence of color patterns among closely related species was greater between sympatric than between allopatric lineages, but only at intermediate levels of sympatry (50%-80% breeding-range overlap). This pattern suggests that closely related species incur costs at intermediate levels of sympatry if they exhibit similar color patterns-costs that could include hybridization, interspecific aggression, competition for signaling space, or ecological interactions that secondarily influence color patterns. The decline in color pattern divergence with further increase in sympatry suggests either the relaxation of divergent selection, increased impediment of gene flow, or an increased role for counteracting selection at higher levels of sympatry. We also found that the differences in color pattern between sympatric and allopatric sister species were greatest at lower latitudes. The global scale and broad taxonomic coverage in our study suggest that the divergence of color patterns between sympatrically breeding closely related species is widespread in birds.
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http://dx.doi.org/10.1086/680206DOI Listing
April 2015

Phylogeography and genetic structure of two Patagonian shag species (Aves: Phalacrocoracidae).

Mol Phylogenet Evol 2014 Mar 10;72:42-53. Epub 2014 Jan 10.

Museo Argentino de Ciencias Naturales "Bernardino Rivadavia", CONICET, Av. Angel Gallardo 470, C1405DJR Ciudad Autónoma de Buenos Aires, Buenos Aires, Argentina.

We compared the phylogeographic and genetic structure of two sympatric shag species, Phalacrocorax magellanicus (rock shag) and Phalacrocorax atriceps (imperial shag), from Patagonia (southern South America). We used multilocus genotypes of nuclear DNA (microsatellite loci) from 324 individuals and mitochondrial DNA sequences (ATPase) from 177 individuals, to evaluate hypotheses related to the effect of physical and non-physical barriers on seabird evolution. Despite sharing many ecological traits, the focal species strongly differ in two key aspects: P. magellanicus has a strong tendency to remain at/near their breeding colonies during foraging trips and the non-breeding season, while P. atriceps exhibits the converse pattern. Both species showed similar mtDNA genetic structure, where colonies from the Atlantic Coast, Pacific Coast and Fuegian region were genetically divergent. We also found similarities in the results of Bayesian clustering analysis of microsatellites, with both species having four clusters. However population differentiation (e.g. Fst, Φst) was higher in P. magellanicus compared to P. atriceps, and average membership probabilities of individuals to specific clusters (Q-values) were also higher in the former. Phalacrocorax magellanicus has strong phylogeographic structure, consistent with the impact of Pleistocene glaciations, with diagnostic haplotypes associated with each of the three mentioned regions. The same pattern was not as evident for P. atriceps. Migration rate estimators were higher for P. atriceps than for P. magellanicus; however both species followed an n-island-like model of gene flow, this implies that dispersal occurs across the continental land mass that separates Atlantic and Pacific Oceans. Our results supported the hypothesis that non-physical barriers are important drivers of the genetic and phylogeographic structure in seabirds, and also that physical barriers constitute effective but not absolute impediments to gene flow.
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http://dx.doi.org/10.1016/j.ympev.2013.12.011DOI Listing
March 2014

Testing for intraspecific postzygotic isolation between cryptic lineages of Pseudacris crucifer.

Ecol Evol 2013 Nov 23;3(14):4621-30. Epub 2013 Oct 23.

Department of Biology, Queen's University Kingston, Ontario, Canada, K7L 3N6.

Phenotypically cryptic lineages appear common in nature, yet little is known about the mechanisms that initiate and/or maintain barriers to gene flow, or how secondary contact between them might influence evolutionary trajectories. The consequences of such contact between diverging lineages depend on hybrid fitness, highlighting the potential for postzygotic isolating barriers to play a role in the origins of biological species. Previous research shows that two cryptic, deeply diverged intraspecific mitochondrial lineages of a North American chorus frog, the spring peeper (Pseudacris crucifer), meet in secondary contact in Southwestern Ontario, Canada. Our study quantified hatching success, tadpole survival, size at metamorphosis, and development time for experimentally generated pure lineage and hybrid tadpoles. Results suggest that lineages differ in tadpole survival and that F1 hybrids may have equal fitness and higher than average mass at metamorphosis compared with pure parental crosses. These findings imply hybrid early life viability may not be the pivotal reproductive isolation barrier helping to maintain lineage boundaries. However, we observed instances of tadpole gigantism, failure to metamorphose, and bent tails in some tadpoles from hybrid families. We also speculate and provide some evidence that apparent advantages or similarities of hybrids compared with pure lineage tadpoles may disappear when tadpoles are raised with competitors of different genetic makeup. This pilot study implies that ecological context and consideration of extrinsic factors may be a key to revealing mechanisms causing negative hybrid fitness during early life stages, a provocative avenue for future investigations on barriers to gene flow among these intraspecific lineages.
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http://dx.doi.org/10.1002/ece3.851DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3867898PMC
November 2013

Extensive sampling of polar bears (Ursus maritimus) in the Northwest Passage (Canadian Arctic Archipelago) reveals population differentiation across multiple spatial and temporal scales.

Ecol Evol 2013 Sep 3;3(9):3152-65. Epub 2013 Aug 3.

Department of Biology, Queen's University Kingston, Ontario, Canada, K7L 3N6 ; División de Ornitología, Museo Argentino de Ciencias Naturales "Bernardino Rivadavia" Avenida. Ángel Gallardo 470, Ciudad de Buenos Aires, Buenos Aires, Argentina, C1405DJR.

As global warming accelerates the melting of Arctic sea ice, polar bears (Ursus maritimus) must adapt to a rapidly changing landscape. This process will necessarily alter the species distribution together with population dynamics and structure. Detailed knowledge of these changes is crucial to delineating conservation priorities. Here, we sampled 361 polar bears from across the center of the Canadian Arctic Archipelago spanning the Gulf of Boothia (GB) and M'Clintock Channel (MC). We use DNA microsatellites and mitochondrial control region sequences to quantify genetic differentiation, estimate gene flow, and infer population history. Two populations, roughly coincident with GB and MC, are significantly differentiated at both nuclear (F ST = 0.01) and mitochondrial (ΦST = 0.47; F ST = 0.29) loci, allowing Bayesian clustering analyses to assign individuals to either group. Our data imply that the causes of the mitochondrial and nuclear genetic patterns differ. Analysis of mtDNA reveals the matrilineal structure dates at least to the Holocene, and is common to individuals throughout the species' range. These mtDNA differences probably reflect both genetic drift and historical colonization dynamics. In contrast, the differentiation inferred from microsatellites is only on the scale of hundreds of years, possibly reflecting contemporary impediments to gene flow. Taken together, our data suggest that gene flow is insufficient to homogenize the GB and MC populations and support the designation of GB and MC as separate polar bear conservation units. Our study also provide a striking example of how nuclear DNA and mtDNA capture different aspects of a species demographic history.
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http://dx.doi.org/10.1002/ece3.662DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3790558PMC
September 2013

The influence of landscape on gene flow in the eastern massasauga rattlesnake (Sistrurus c. catenatus): insight from computer simulations.

Mol Ecol 2013 Sep 29;22(17):4483-98. Epub 2013 Jul 29.

Department of Biology, Queen's University, Kingston, ON, Canada, K7L 3N6.

Understanding how gene flow shapes contemporary population structure requires the explicit consideration of landscape composition and configuration. New landscape genetic approaches allow us to link such heterogeneity to gene flow within and among populations. However, the attribution of cause is difficult when landscape features are spatially correlated, or when genetic patterns reflect past events. We use spatial Bayesian clustering and landscape resistance analysis to identify the landscape features that influence gene flow across two regional populations of the eastern massasauga rattlesnake, Sistrurus c. catenatus. Based on spatially explicit simulations, we inferred how habitat distribution modulates gene flow and attempted to disentangle the effects of spatially confounded landscape features. We found genetic clustering across one regional landscape but not the other, and also local differences in the effect of landscape on gene flow. Beyond the effects of isolation-by-distance, water bodies appear to underlie genetic differentiation among individuals in one regional population. Significant effects of roads were additionally detected locally, but these effects are possibly confounded with the signal of water bodies. In contrast, we found no signal of isolation-by-distance or landscape effects on genetic structure in the other regional population. Our simulations imply that these local differences have arisen as a result of differences in population density or tendencies for juvenile rather than adult dispersal. Importantly, our simulations also demonstrate that the ability to detect the consequences of contemporary anthropogenic landscape features (e.g. roads) on gene flow may be compromised when long-standing natural features (e.g. water bodies) co-exist on the landscape.
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http://dx.doi.org/10.1111/mec.12411DOI Listing
September 2013

Changes in breeding phenology of eastern Ontario frogs over four decades.

Ecol Evol 2013 Apr 26;3(4):835-45. Epub 2013 Feb 26.

Department of Biology, Queen's University Kingston, Canada.

Global climate change has been implicated in phenological shifts for a variety of taxa. Amphibian species in particular are sensitive to changes in their environment due to their biphasic life history and restricted reproductive requirements. Previous research has shown that not all temperate amphibian species respond similarly to the same suite of climatic or environmental cues, nor are individual species necessarily uniform in their responses across their range. We examined both the timing of spring emergence and calling phenology of eight anuran species in southeastern Ontario, Canada, using an approximately 40-year dataset of historical records of amphibian activity. Rana pipiens was the only species out of eight considered to emerge significantly earlier, by an estimated 22 days over four decades. Both R. pipiens and Bufo americanus have advanced initiation of calling over a four-decade span significantly earlier by an estimated 37.2 and 19.2 days, respectively. Rana sylvatica showed a trend toward earlier emergence by 19 days, whereas we did not detect changes in emergence phenology for the remaining five species. This significant shift in breeding behavior for two species correlates to significant regional increases in spring temperatures of an estimated 2.7-2.8°C overall over four decades. Our study suggests that local temperature increases have affected the timing of emergence and the onset of calling activity in some Ontario anuran species. Global decline or range shifts ultimately may be related to changes in reproductive behavior and timing mediated by shifting climate.
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http://dx.doi.org/10.1002/ece3.501DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3631398PMC
April 2013

Early Miocene origin and cryptic diversification of South American salamanders.

BMC Evol Biol 2013 Mar 4;13:59. Epub 2013 Mar 4.

Department of Biology, Queen's University, Kingston, Ontario, Canada.

Background: The currently recognized species richness of South American salamanders is surprisingly low compared to North and Central America. In part, this low richness may be due to the salamanders being a recent arrival to South America. Additionally, the number of South American salamander species may be underestimated because of cryptic diversity. The aims of our present study were to infer evolutionary relationships, lineage diversity, and timing of divergence of the South American Bolitoglossa using mitochondrial and nuclear sequence data from specimens primarily from localities in the Andes and upper Amazon Basin. We also estimated time of colonization of South America to test whether it is consistent with arrival via the Panamanian Isthmus, or land bridge connection, at its traditionally assumed age of 3 million years.

Results: Divergence time estimates suggest that Bolitoglossa arrived in South America from Central America by at least the Early Miocene, ca. 23.6 MYA (95% HPD 15.9-30.3 MYA), and subsequently diversified. South American salamanders of the genus Bolitoglossa show strong phylogeographic structure at fine geographic scales and deep divergences at the mitochondrial gene cytochrome b (Cytb) and high diversity at the nuclear recombination activating gene-1 (Rag1). Species often contain multiple genetically divergent lineages that are occasionally geographically overlapping. Single specimens from two southeastern localities in Ecuador are sister to the equatoriana-peruviana clade and genetically distinct from all other species investigated to date. Another single exemplar from the Andes of northwestern Ecuador is highly divergent from all other specimens and is sister to all newly studied samples. Nevertheless, all sampled species of South American Bolitoglossa are members of a single clade that is one of several constituting the subgenus Eladinea, one of seven subgenera in this large genus.

Conclusions: The ancestors of South American salamanders likely arrived at least by the Early Miocene, well before the completion of the Late Pliocene Panamanian land bridge (widely accepted as ca. 3 MYA). This date is in agreement with recent, controversial, arguments that an older, perhaps short-lived, land connection may have existed between South America and present-day Panama 23-25 MYA. Since its arrival in South America, Bolitoglossa has diversified more extensively than previously presumed and currently includes several cryptic species within a relatively small geographic area. Rather than two upper Amazonian species currently recorded for this region, we propose that at least eight should be recognized, although these additional lineages remain to be formally described.
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http://dx.doi.org/10.1186/1471-2148-13-59DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3602097PMC
March 2013

Continental phylogeography of an ecologically and morphologically diverse Neotropical songbird, Zonotrichia capensis.

BMC Evol Biol 2013 Mar 1;13:58. Epub 2013 Mar 1.

Department of Biology, Queen's University, Kingston, ON, K7L 3N6, Canada.

Background: The Neotropics are exceptionally diverse, containing roughly one third of all extant bird species on Earth. This remarkable species richness is thought to be a consequence of processes associated with both Andean orogenesis throughout the Tertiary, and climatic fluctuations during the Quaternary. Phylogeographic studies allow insights into how such events might have influenced evolutionary trajectories of species and ultimately contribute to a better understanding of speciation. Studies on continentally distributed species are of particular interest because different populations of such taxa may show genetic signatures of events that impacted the continent-wide biota. Here we evaluate the genealogical history of one of the world's most broadly-distributed and polytypic passerines, the rufous-collared sparrow (Zonotrichia capensis).

Results: We obtained control region DNA sequences from 92 Zonotrichia capensis individuals sampled across the species' range (Central and South America). Six additional molecular markers, both nuclear and mitochondrial, were sequenced for a subset of individuals with divergent control region haplotypes. Median-joining network analysis, and Bayesian and maximum parsimony phylogenetic analyses all recovered three lineages: one spanning Middle America, the Dominican Republic, and north-western South America; one encompassing the Dominican Republic, Roraima (Venezuela) and La Paz (Bolivia) south to Tierra del Fuego, Argentina; and a third, including eastern Argentina and Brazil. Phylogenetic analyses suggest that the Middle American/north-western South American clade is sister to the remaining two. Bayesian and maximum likelihood coalescent simulations used to study lineage demographic history, diversification times, migration rates and population expansion together suggested that diversification of the three lineages occurred rapidly during the Pleistocene, with negligible gene flow, leaving genetic signatures of population expansions.

Conclusions: The Pleistocene history of the rufous-collared sparrow involved extensive range expansion from a probable Central American origin. Its remarkable morphological and behavioral diversity probably represents recent responses to local conditions overlying deeper patterns of lineage diversity, which are themselves produced by isolation and the history of colonization of South America.
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http://dx.doi.org/10.1186/1471-2148-13-58DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3632491PMC
March 2013

Advances in linking wintering migrant birds to their breeding-ground origins using combined analyses of genetic and stable isotope markers.

PLoS One 2012 20;7(8):e43627. Epub 2012 Aug 20.

Department of Biology, Queen's University, Kingston, Ontario, Canada.

An enduring problem in avian ecology and conservation is linking breeding and wintering grounds of migratory species. As migratory species and populations vary in the degree to which individuals from distinct breeding locales mix on stop-over sites and wintering grounds, establishing migratory connectivity informs our understanding of population demography and species management. We present a new Bayesian approach for inferring breeding grounds of wintering birds of unknown origins in North America. We incorporate prior information from analysis of genetic markers into geographic origin assignment based upon stable-hydrogen isotope analysis of feathers (δ(2)H(f)), using the Loggerhead Shrike (Lanius ludovicianus). Likely geographic origins derived from analyses of DNA microsatellites were used as priors for Bayesian analyses in which birds were assigned to a breeding-ground origin using their δ(2)H(f) values. As with most applications of Bayesian methods, our approach greatly improved the results (i.e. decreased the size of the potential area of origin). Area of origin decreased by 3 to 5-fold on average, but ranged up to a 10-fold improvement. We recommend this approach in future studies of migratory connectivity and suggest that our methodology could be applied more broadly to the study of dispersal, sources of productivity of migratory populations, and a range of evolutionary phenomena.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0043627PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3423384PMC
January 2013

Evolution of mitochondrial-encoded cytochrome oxidase subunits in endothermic fish: the importance of taxon-sampling in codon-based models.

Mol Phylogenet Evol 2012 Jun 1;63(3):679-84. Epub 2012 Mar 1.

Department of Biology, Queen's University, Kingston, Ontario, Canada K7L 3N6.

While endothermy is ubiquitous in birds and mammals, it is not exclusive to these most recently arisen vertebrate classes. The ability to warm specific organs and/or tissues above ambient temperature (regional endothermy) has evolved at least three times in phylogentically discrete fish lineages: lamnid sharks (Lamnidae), tunas (Scombridae) and billfishes (Istiophoridae and Xiphidae). Given the links between endothermy and metabolic rate, we looked for evidence of convergent molecular evolution in mtDNA-encoded cytochrome c oxidase (COX) subunits in each of these discrete lineages. We found no evidence that the endothermic phenotype in fishes is driven or accompanied by molecular convergence. Though we found little evidence for positively-selected sites in any of the lineages in any subunit, the conclusions were sensitive to the choice of maximum-likelihood model. Several sites identified by Naïve Empirical Bayes (NEB) were not found when Bayes Empirical Bayes (BEB) was employed. As well, conclusions were profoundly influenced by taxon-sampling. Several of the putative sites of positive selection in COX II were no longer apparent as we augmented taxon sampling. The lack of convergent molecular evolution in these remarkable taxa, combined with the profound influence of model choice and taxon sampling provide a cautionary note on the use of rates of non-synonymous to synonymous mutations (dN/dS) to explore questions of the evolution of physiological function.
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http://dx.doi.org/10.1016/j.ympev.2012.02.012DOI Listing
June 2012

Rapid phenotypic evolution during incipient speciation in a continental avian radiation.

Proc Biol Sci 2012 May 30;279(1734):1847-56. Epub 2011 Nov 30.

División de Ornitología, Museo Argentino de Ciencias Naturales Bernardino Rivadavia, Avenida Ángel Gallardo 470, Ciudad de Buenos Aires C1405DJR, Buenos Aires, Argentina.

Adaptive radiations have helped shape how we view animal speciation, particularly classic examples such as Darwin's finches, Hawaiian fruitflies and African Great Lakes cichlids. These 'island' radiations are comparatively recent, making them particularly interesting because the mechanisms that caused diversification are still in motion. Here, we identify a new case of a recent bird radiation within a continentally distributed species group; the capuchino seedeaters comprise 11 Sporophila species originally described on the basis of differences in plumage colour and pattern in adult males. We use molecular data together with analyses of male plumage and vocalizations to understand species limits of the group. We find marked phenotypic variation despite lack of mitochondrial DNA monophyly and few differences in other putatively neutral nuclear markers. This finding is consistent with the group having undergone a recent radiation beginning in the Pleistocene, leaving genetic signatures of incomplete lineage sorting, introgressive hybridization and demographic expansions. We argue that this apparent uncoupling between neutral DNA homogeneity and phenotypic diversity is expected for a recent group within the framework of coalescent theory. Finally, we discuss how the ecology of open habitats in South America during the Pleistocene could have helped promote this unique and ongoing radiation.
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http://dx.doi.org/10.1098/rspb.2011.2170DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3297458PMC
May 2012

A molecular phylogeny of the Sierra-Finches (Phrygilus, Passeriformes): extreme polyphyly in a group of Andean specialists.

Mol Phylogenet Evol 2011 Nov 23;61(2):521-33. Epub 2011 Jul 23.

División de Ornitología, Museo Argentino de Ciencias Naturales Bernardino Rivadavia, Av. Ángel Gallardo 470, Ciudad de Buenos Aires, C1405DJR Buenos Aires, Argentina.

The unparalleled avian diversity of the Neotropics has long been argued to be in large part the evolutionary consequence of the incredible habitat diversity and rugged topography of the Andes mountains. Various scenarios have been proposed to explain how the Andean context could have generated lineage diversification (e.g. vicariant speciation or parapatric speciation across vertical ecological gradients), yet further study on Andean taxa is needed to reveal the relative importance of the different processes. Here we use mitochondrial and nuclear DNA sequences to derive the first phylogenetic hypothesis for Phrygilus (Sierra-Finches), one of the most species-rich genera of mainly Andean passerines. We find strong evidence that the genus is polyphyletic, comprising four distantly related clades with at least nine other genera interspersed between them (Acanthidops, Catamenia, Diglossa, Haplospiza, Idiopsar, Melanodera, Rowettia, Sicalis and Xenodacnis). These four Phrygilus clades coincide with groups previously established mainly on the basis of plumage characters, suggesting single evolutionary origins for each of these. We consider the history of diversification of each clade, analyzing the timing of splitting events, ancestral reconstruction of altitudinal ranges and current geographical distributions. Phrygilus species origins date mainly to the Pleistocene, with representatives diversifying within, out of, and into the Andes. Finally, we explored whether Phrygilus species, especially those with broad altitudinal and latitudinal Andean distributions, showed phylogeographic structure. Our best-sampled taxon (Phrygilus fruticeti) exhibited no clear pattern; however, we found deep genetic splits within other surveyed species, with Phrygilus unicolor being the most extreme case and deserving of further research.
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http://dx.doi.org/10.1016/j.ympev.2011.07.011DOI Listing
November 2011

DNA barcodes provide new evidence of a recent radiation in the genus Sporophila (Aves: Passeriformes).

Mol Ecol Resour 2010 May 9;10(3):449-58. Epub 2009 Dec 9.

División de Ornitología, Museo Argentino de Ciencias Naturales "Bernardino Rivadavia", Av. Ángel Gallardo 470, Ciudad de Buenos Aires, C1405DJR Buenos Aires, Argentina Department of Integrative Biology, Biodiversity Institute of Ontario, University of Guelph, 50 Stone Road East, Guelph, ON, Canada N1G 2W1 Department of Biology, Queen's University, 116 Barrie Street, Kingston, ON, Canada K7L 3N6.

The capuchinos are a group of birds in the genus Sporophila that has apparently radiated recently, as evidenced by their lack of mitochondrial genetic diversity. We obtained cytochrome c oxidase I (COI) sequences (or DNA barcodes) for the 11 species of the group and various outgroups. We compared the patterns of COI variability of the capuchinos with those of the largest barcode data set from neotropical birds currently available (500 species representing 51% of avian richness in Argentina), and subjected COI sequences to neighbour-joining, maximum parsimony and Bayesian phylogenetic analyses as well as statistical parsimony network analysis. A clade within the capuchinos, the southern capuchinos, showed higher intraspecific and lower interspecific divergence than the remaining Argentine species. As most of the southern capuchinos shared COI haplotypes and pairwise distances within species were in many cases higher than distances between them, the phylogenetic affinities within the group remained unresolved. The observed genetic pattern is consistent with both incomplete lineage sorting and gene flow between species. The southern capuchinos constitute the only large group of species among the neotropical birds barcoded so far that are inseparable when using DNA barcodes, and one of few multispecies avian groups known to lack reciprocal monophyly. Extending the analysis to rapidly evolving nuclear and mitochondrial markers will be crucial to understanding this radiation. Apart from giving insights into the evolution of the capuchinos, this study shows how DNA barcoding can rapidly flag species or groups of species worthy of deeper study.
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http://dx.doi.org/10.1111/j.1755-0998.2009.02799.xDOI Listing
May 2010

Phylogeography and genetic structure of the red-legged partridge (Alectoris rufa): more evidence for refugia within the Iberian glacial refugium.

Mol Ecol 2011 Jun 3;20(12):2628-42. Epub 2011 May 3.

Instituto de Investigación en Recursos Cinegéticos, IREC (CSIC, UCLM, JCCM), Ronda de Toledo s/n, 13005-Ciudad Real, Spain.

The Pleistocene climatic oscillations promoted the diversification in avian species during the last glacial period. The red-legged partridge (Alectoris rufa, Family Phasianidae) has a large natural distribution extending from the Mediterranean to humid temperate zones. However, the genetic structure for this species is unknown. The present study investigates the phylogeography, genetic structure and demographic history of A. rufa across its distribution, employing both mitochondrial DNA control region sequences and nuclear microsatellite loci. Our results propose that this species was greatly affected by Pleistocene glaciations. The mismatch analyses suggest that the current populations resulted from post-glacial expansion and subsequent differentiation resulting in five diagnosable genetic clusters: Southwestern, Central-eastern, Northwestern, Balearic and French and Italian. Further, we found evidence of three glacial refugia within the currently recognized Iberian glacial refugium. The intraspecific structure revealed by both maternal and biparental phylogeographic analyses was not resolved in the phylogenetic analyses. Based on all considerations, we recommended that five management units be recognized.
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http://dx.doi.org/10.1111/j.1365-294X.2011.05111.xDOI Listing
June 2011
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