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Proceedings of the National Academy of Sciences of the United States of America | 2014

Species formation by host shifting in avian malaria parasites

Robert E. Ricklefs; Diana C. Outlaw; Maria Svensson-Coelho; Matthew C. I. Medeiros; Vincenzo A. Ellis; Steven C. Latta

Significance Emerging infectious diseases pose threats to humans and livestock, but little is known about the general propensity of parasitic organisms to shift between hosts or the role of host shifting in the diversification of parasite lineages. The malaria parasites of contemporary vertebrate species descended from a common ancestor, likely after the diversification of their major host taxa, requiring rapid speciation and shifting between hosts across large host–taxonomic distances. Examination of sister lineages of avian malaria parasites in the New World suggests that such host shifting is common and often leads to the origin of new evolutionary lineages of parasites. The malaria parasites (Apicomplexa: Haemosporida) of birds are believed to have diversified across the avian host phylogeny well after the origin of most major host lineages. Although many symbionts with direct transmission codiversify with their hosts, mechanisms of species formation in vector-borne parasites, including the role of host shifting, are poorly understood. Here, we examine the hosts of sister lineages in a phylogeny of 181 putative species of malaria parasites of New World terrestrial birds to determine the role of shifts between host taxa in the formation of new parasite species. We find that host shifting, often across host genera and families, is the rule. Sympatric speciation by host shifting would require local reproductive isolation as a prerequisite to divergent selection, but this mechanism is not supported by the generalized host-biting behavior of most vectors of avian malaria parasites. Instead, the geographic distribution of individual parasite lineages in diverse hosts suggests that species formation is predominantly allopatric and involves host expansion followed by local host–pathogen coevolution and secondary sympatry, resulting in local shifting of parasite lineages across hosts.


The Auk | 2007

MOLECULAR SYSTEMATICS AND HISTORICAL BIOGEOGRAPHY OF THE ROCK-THRUSHES (MUSCICAPIDAE: MONTICOLA)

Robert K. Outlaw; Gary Voelker; Diana C. Outlaw

Abstract The genus Monticola consists of 13 putative species with distributions throughout Eurasia and the sub-Saharan region of Africa. As such, this genus provides an excellent model with which to explore historical intercontinental movements and forces driving speciation in southern Africa. To address these questions, we reconstructed a hypothesis of species relationships using the mitochondrial ND2 and cytochrome-b genes. Monticola forms a well-supported, monophyletic clade within the avian family Muscicapidae. Our results support previous studies suggesting that the Malagasy genus Pseudocossyphus be subsumed into Monticola, and suggest that several of the Malagasy species (notably M. bensoni and M. erythronotus) are not valid. Sequence data, along with morphological and distributional evidence, support the elevation of M. pretoriae to species status. Historical biogeographic analyses suggest an area of origin for Monticola in the arid region of northern Africa plus Saudi Peninsula or the African savanna, or both. Determination of speciation timing suggests that Monticola arose ≈5.5 mya, with subsequent lineage splits occurring throughout the Pliocene and Pleistocene. We propose that climate-driven ecological vicariance as well as dispersal were important in the biogeographic history of this group and are responsible for present-day species relationships and distributions. Systématique moléculaire et biogéographie historique des monticoles (Muscicapidae: Monticola)


Trends in Parasitology | 2013

How can we determine the molecular clock of malaria parasites

Staffan Bensch; Olof Hellgren; Asta Križanauskienė; Vaidas Palinauskas; Gediminas Valkiūnas; Diana C. Outlaw; Robert E. Ricklefs

The association of contemporary hosts and their parasites might reflect either cospeciation or more recent shifts among existing hosts. Cospeciation implies that lineages of hosts and parasites diverge in parallel at the same time, but testing this prediction requires time-calibrated phylogenies, which are particularly difficult to obtain in organisms that leave few fossils. It has successively become clear that host shifts have been frequent in the evolutionary history of malaria parasites, but dating these host shifts cannot be done without calibrated phylogenies. Hence, it remains unresolved how long contemporary hosts and vectors have been coevolving with their malaria parasites. This review addresses conflicting rate estimates of molecular evolution and suggests research directions to aid dating diversification events in malaria parasites.


Parasitology | 2015

Differential patterns of molecular evolution among Haemosporidian parasite groups

Robert K. Outlaw; Brian A. Counterman; Diana C. Outlaw

Malaria parasites have had profound effects on human populations for millennia, but other terrestrial vertebrates are impacted by malaria as well. Entire species of birds have been driven to extinction, and many others are threatened by population declines. Recent studies have shown that host-switching is quite common among malaria parasite lineages, and these switches often involve a significant shift in the environment in which the parasites find themselves, including nucleated vs non-nucleated red blood cells and red vs white blood cells. Therefore, it is important to understand how parasites adapt to these different host environments. The mitochondrial cytochrome b (cyt b) gene shows evidence of adaptive molecular evolution among malaria parasite groups, putatively because of its critical role in the electron transport chain (ETC) in cellular metabolism. Two hypotheses were addressed here: (1) mitochondrial components of the ETC (cyt b and cytochrome oxidase 1 [COI]) should show evidence of adaptive evolution (i.e., selection) and (2) selection should be evident in host switches. Overall we found a signature of constraint (e.g., purifying selection) across the four genes included here, but we also found evidence of positive selection associated with host switches in cyt b and, surprisingly, in (apicoplast) caseinolytic protease C. These results suggest that evidence of selection should be widespread across these parasite genomes.


Molecular Phylogenetics and Evolution | 2015

Phylogeny and biogeography of Ficedula flycatchers (Aves: Muscicapidae): novel results from fresh source material.

Robert G. Moyle; Peter A. Hosner; Andrew W. Jones; Diana C. Outlaw

The avian genus Ficedula has been a model system for studying speciation, genomics, biogeography, and the evolution of migratory behavior. However, no multi-locus molecular phylogenetic hypothesis exists for the genus. We expanded taxon and character sampling over previous studies and produced a robust hypothesis of relationships for the genus. Many previous findings, such as the inclusion of Muscicapella and exclusion of Ficedula monileger from the genus, were verified, but many relationships differed compared to previous work. Some of the differences were due to increased sampling, but others were due to problematic sequence data produced from DNA extracted from historical museum specimens. The new phylogenetic hypothesis resulted in a simpler biogeographic scenario with fewer transitions between regions and fewer transitions between seasonally migratory and resident character states. Notably, all species endemic to the Philippines and Wallacea formed a clade, which included Ficedula dumetoria of the Sunda Shelf and Lesser Sundas. In addition, Ficedula hyperythra was not monophyletic; samples from Philippine populations formed a clade distantly related to a clade that comprised all other sampled populations.


Parasitology | 2017

Diversity and distribution of avian haemosporidians in sub-Saharan Africa: an inter-regional biogeographic overview

Diana C. Outlaw; Johanna A. Harvey; Sergei V. Drovetski; Gary Voelker

The diversity of avian malaria parasites is much greater than 20th century morphologists realized and virtually every study in this field in the last 15 years has uncovered previously undocumented diversity at multiple levels within the taxonomic hierarchy. Despite this explosion of knowledge, there remain vast sampling gaps, both geographically and host-taxonomically, which makes characterizing patterns of diversity extremely challenging. Here, we summarize the current state of knowledge of sub-Saharan African avian malaria parasite diversity, focusing on avian hosts endemic to Africa. The relative proportions of the parasite genera included here, Plasmodium, Haemoproteus (including Parahaemoproteus) and Leucocytozoon, varied between regions, in part due to habitat preferences of the insect vectors of these genera, and in part we believe due to sampling bias. Biogeographic regions of sub-Saharan Africa harbour about the same proportion of endemic to shared parasite lineages, but there appears to be no phylogenetic structuring across regions. Our results highlight the sampling problem that must be addressed if we are to have a detailed understanding of parasite diversity in Africa. Without broad sampling within and across regions and hosts, using both molecular tools and microscopy, conclusions about parasite diversity, host-parasite interactions or even transmission dynamics remain extremely limited.


Molecular Phylogenetics and Evolution | 2017

A novel Haemosporida clade at the rank of genus in North American cranes (Aves: Gruiformes)

Miranda R. Bertram; Sarah A. Hamer; Barry K. Hartup; K.F. Snowden; Matthew C. I. Medeiros; Diana C. Outlaw; Gabriel L. Hamer

The unicellular blood parasites in the order Haemosporida are highly diverse, infect many vertebrates, are responsible for a large disease burden among humans and animals, and have reemerged as an important model system to understand the evolutionary and ecological dynamics of host-parasite interactions. The phylogenetics and systematics of Haemosporida are limited by poor sampling of different vertebrate host taxa. We surveyed the Haemosporida of wild whooping cranes (Grus americana) and sandhill cranes (Grus canadensis) (Aves: Gruiformes) using a combination of morphological and molecular approaches. We identified Haemoproteus antigonis in blood smears based on published morphological descriptions. Phylogenetic analysis based on partial cytochrome b (cytb) and cytochrome oxidase (coI) sequences placed H. antigonis parasites in a novel clade, distinct from all avian Haemosporida genera for which cytb and/or coI sequences are available. Molecular clock and divergence estimates suggest this crane clade may represent a new genus. This is the first molecular description of H. antigonis and the first report of H. antigonis in wild whooping cranes, an endangered bird in North America. Further sampling of Haemosporida, especially from hosts of the Gruiformes and other poorly sampled orders, will help to resolve the relationship of the H. antigonis clade to other avian Haemosporida genera. Our study highlights the potential of sampling neglected host species to discover novel lineages of diverse parasite groups.


Parasitology | 2014

Species limits in avian malaria parasites (Haemosporida): how to move forward in the molecular era

Diana C. Outlaw; Robert E. Ricklefs


Journal of Biogeography | 2017

Avian migration and the distribution of malaria parasites in New World passerine birds

Robert E. Ricklefs; Matthew Medeiros; Vincenzo A. Ellis; Maria Svensson-Coelho; John G. Blake; Bette A. Loiselle; Letícia Soares; Alan Fecchio; Diana C. Outlaw; Peter P. Marra; Steven C. Latta; Gediminas Valkiūnas; Olof Hellgren; Staffan Bensch


Contributions to Zoology | 2011

Morphological evolution of some migratory Ficedula flycatchers

Diana C. Outlaw

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Robert E. Ricklefs

University of Missouri–St. Louis

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Maria Svensson-Coelho

University of Missouri–St. Louis

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Matthew C. I. Medeiros

University of Missouri–St. Louis

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Robert K. Outlaw

Mississippi State University

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Vincenzo A. Ellis

University of Missouri–St. Louis

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