Publications by authors named "Matthew L Aardema"

22 Publications

  • Page 1 of 1

Persistence and expansion of cryptic endangered red wolf genomic ancestry along the American Gulf coast.

Mol Ecol 2021 Sep 29. Epub 2021 Sep 29.

Veterinary Integrative Biosciences, Texas A&M University, College Station, Texas, USA.

Admixture and introgression play a critical role in adaptation and genetic rescue that has only recently gained a deeper appreciation. Here, we explored the geographical and genomic landscape of cryptic ancestry of the endangered red wolf that persists within the genome of a ubiquitous sister taxon, the coyote, all while the red wolf has been extinct in the wild since the early 1980s. We assessed admixture across 120,621 single nucleotiode polymorphism (SNP) loci genotyped in 293 canid genomes. We found support for increased red wolf ancestry along a west-to-east gradient across the southern United States associated with historical admixture in the past 100 years. Southwestern Louisiana and southeastern Texas, the geographical zone where the last red wolves were known prior to extinction in the wild, contained the highest and oldest levels of red wolf ancestry. Further, given the paucity of inferences based on chromosome types, we compared patterns of ancestry on the X chromosome and autosomes. We additionally aimed to explore the relationship between admixture timing and recombination rate variation to investigate gene flow events. We found that X-linked regions of low recombination rates were depleted of introgression, relative to the autosomes, consistent with the large X effect and enrichment with loci involved in maintaining reproductive isolation. Recombination rate was positively correlated with red wolf ancestry across coyote genomes, consistent with theoretical predictions. The geographical and genomic extent of cryptic red wolf ancestry can provide novel genomic resources for recovery plans targeting the conservation of the endangered red wolf.
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http://dx.doi.org/10.1111/mec.16200DOI Listing
September 2021

Genomic signatures of spatially divergent selection at clownfish range margins.

Proc Biol Sci 2021 06 9;288(1952):20210407. Epub 2021 Jun 9.

Department of Ecology, Evolution and Natural Resources, Rutgers University, 14 College Farm Road, New Brunswick, NJ 08901, USA.

Understanding how evolutionary forces interact to drive patterns of selection and distribute genetic variation across a species' range is of great interest in ecology and evolution, especially in an era of global change. While theory predicts how and when populations at range margins are likely to undergo local adaptation, empirical evidence testing these models remains sparse. Here, we address this knowledge gap by investigating the relationship between selection, gene flow and genetic drift in the yellowtail clownfish, from the core to the northern periphery of the species range. Analyses reveal low genetic diversity at the range edge, gene flow from the core to the edge and genomic signatures of local adaptation at 56 single nucleotide polymorphisms in 25 candidate genes, most of which are significantly correlated with minimum annual sea surface temperature. Several of these candidate genes play a role in functions that are upregulated during cold stress, including protein turnover, metabolism and translation. Our results illustrate how spatially divergent selection spanning the range core to the periphery can occur despite the potential for strong genetic drift at the range edge and moderate gene flow from the core populations.
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http://dx.doi.org/10.1098/rspb.2021.0407DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8187997PMC
June 2021

The urban-adapted underground mosquito Culex pipiens form molestus maintains exogenously influenceable circadian rhythms.

J Exp Biol 2021 05 24;224(10). Epub 2021 May 24.

Department of Biology, Montclair State University, 1 Normal Avenue, Montclair, NJ 07043, USA.

Genes known to affect circadian rhythms (i.e. 'clock genes') also influence the photoperiodic induction of overwintering reproductive diapause in the northern house mosquito, Culex pipiens f. pipiens. This suggests that molecular changes in one or more clock genes could contribute to the inability to diapause in a second form of this mosquito, Culex pipiens f. molestus. Temperate populations of Cx. pipiens f. molestus inhabit underground locations generally devoid of predictable photoperiods. For this reason, there could be limited fitness consequences if the hypothesized molecular changes to its clock genes also eliminated this mosquito's ability to regulate circadian rhythms in response to photoperiod variation. Here, we demonstrate that in contrast to this prediction, underground derived Cx. pipiens f. molestus retain exogenously influenceable circadian rhythms. Nonetheless, our genetic analyses indicate that the gene Helicase domino (dom) has a nine-nucleotide, in-frame deletion specific to Cx. pipiens f. molestus. Previous work has shown that splice variants in this gene differentially influence circadian behavior in Drosophila melanogaster. We also find derived, non-synonymous single nucleotide polymorphisms (SNPs) in eight genes that may also affect circadian rhythms and/or diapause induction in Cx. pipiens f. molestus. Finally, four putative circadian genes were found to have no quantifiable expression during any examined life stage, suggesting potential regulatory effects. Collectively, our findings indicate that the distinct, but molecularly interconnected life-history traits of diapause induction and circadian rhythms are decoupled in Cx. pipiens f. molestus and suggest this taxon may be a valuable tool for exploring exogenously influenced phenotypes in mosquitoes more broadly.
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http://dx.doi.org/10.1242/jeb.242231DOI Listing
May 2021

Can public online databases serve as a source of phenotypic information for Cannabis genetic association studies?

PLoS One 2021 23;16(2):e0247607. Epub 2021 Feb 23.

Sackler Institute for Comparative Genomics, American Museum of Natural History, New York, New York, United States of America.

The use of Cannabis is gaining greater social acceptance for its beneficial medicinal and recreational uses. With this acceptance has come new opportunities for crop management, selective breeding, and the potential for targeted genetic manipulation. However, as an agricultural product Cannabis lags far behind other domesticated plants in knowledge of the genes and genetic variation that influence plant traits of interest such as growth form and chemical composition. Despite this lack of information, there are substantial publicly available resources that document phenotypic traits believed to be associated with particular Cannabis varieties. Such databases could be a valuable resource for developing a greater understanding of genes underlying phenotypic variation if combined with appropriate genetic information. To test this potential, we collated phenotypic data from information available through multiple online databases. We then produced a Cannabis SNP database from 845 strains to examine genome wide associations in conjunction with our assembled phenotypic traits. Our goal was not to locate Cannabis-specific genetic variation that correlates with phenotypic variation as such, but rather to examine the potential utility of these databases more broadly for future, explicit genome wide association studies (GWAS), either in stand-alone analyses or to complement other types of data. For this reason, we examined a very broad array of phenotypic traits. In total, we performed 201 distinct association tests using web-derived phenotype data appended to 290 uniquely named Cannabis strains. Our results indicated that chemical phenotypes, such as tetrahydrocannabinol (THC) and cannabidiol (CBD) content, may have sufficiently high-quality information available through web-based sources to allow for genetic association inferences. In many cases, variation in chemical traits correlated with genetic variation in or near biologically reasonable candidate genes, including several not previously implicated in Cannabis chemical variation. As with chemical phenotypes, we found that publicly available data on growth traits such as height, area of growth, and floral yield may be precise enough for use in future association studies. In contrast, phenotypic information for subjective traits such as taste, physiological affect, neurological affect, and medicinal use appeared less reliable. These results are consistent with the high degree of subjectivity for such trait data found on internet databases, and suggest that future work on these important but less easily quantifiable characteristics of Cannabis may require dedicated, controlled phenotyping.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0247607PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7901747PMC
August 2021

Genomic Analysis of the Only Blind Cichlid Reveals Extensive Inactivation in Eye and Pigment Formation Genes.

Genome Biol Evol 2020 08;12(8):1392-1406

Department of Ichthyology, American Museum of Natural History, New York, New York.

Trait loss represents an intriguing evolutionary problem, particularly when it occurs across independent lineages. Fishes in light-poor environments often evolve "troglomorphic" traits, including reduction or loss of both pigment and eyes. Here, we investigate the genomic basis of trait loss in a blind and depigmented African cichlid, Lamprologus lethops, and explore evolutionary forces (selection and drift) that may have contributed to these losses. This species, the only known blind cichlid, is endemic to the lower Congo River. Available evidence suggests that it inhabits deep, low-light habitats. Using genome sequencing, we show that genes related to eye formation and pigmentation, as well as other traits associated with troglomorphism, accumulated inactivating mutations rapidly after speciation. A number of the genes affected in L. lethops are also implicated in troglomorphic phenotypes in Mexican cavefish (Astyanax mexicanus) and other species. Analysis of heterozygosity patterns across the genome indicates that L. lethops underwent a significant population bottleneck roughly 1 Ma, after which effective population sizes remained low. Branch-length tests on a subset of genes with inactivating mutations show little evidence of directional selection; however, low overall heterozygosity may reduce statistical power to detect such signals. Overall, genome-wide patterns suggest that accelerated genetic drift from a severe bottleneck, perhaps aided by directional selection for the loss of physiologically expensive traits, caused inactivating mutations to fix rapidly in this species.
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http://dx.doi.org/10.1093/gbe/evaa144DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7502198PMC
August 2020

Updating the Bibliography of Interbreeding among Canis in North America.

J Hered 2020 05;111(3):249-262

Department of Biology, Montclair State University, Montclair, NJ.

This bibliography provides a collection of references that documents the evolution of studies evidencing interbreeding among Canis species in North America. Over the past several decades, advances in biology and genomic technology greatly improved our ability to detect and characterize species interbreeding, which has significance for understanding species in a changing landscape as well as for endangered species management. This bibliography includes a discussion within each category of interbreeding, the timeline of developing evidence, and includes a review of past research conducted on experimental crosses. Research conducted in the early 20th century is rich with detailed records and photographs of hybrid offspring development and behavior. With the progression of molecular methods, studies can estimate historical demographic parameters and detect chromosomal patterns of ancestry. As these methods continue to increase in accessibility, the field will gain a deeper and richer understanding of the evolutionary history of North American Canis.
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http://dx.doi.org/10.1093/jhered/esaa004DOI Listing
May 2020

Global evaluation of taxonomic relationships and admixture within the Culex pipiens complex of mosquitoes.

Parasit Vectors 2020 Jan 8;13(1). Epub 2020 Jan 8.

Division of Invertebrate Zoology, American Museum of Natural History, New York, NY, USA.

Background: Within the Culex pipiens mosquito complex, there are six contemporarily recognized taxa: Cx. quinquefasciatus, Cx. pipiens f. pipiens, Cx. pipiens f. molestus, Cx. pipiens pallens, Cx. australicus and Cx. globocoxitus. Many phylogenetic aspects within this complex have eluded resolution, such as the relationship of the two Australian endemic taxa to the other four members, as well as the evolutionary origins and taxonomic status of Cx. pipiens pallens and Cx. pipiens f. molestus. Ultimately, insights into lineage relationships within the complex will facilitate a better understanding of differential disease transmission by these mosquitoes. To this end, we have combined publicly available data with our own sequencing efforts to examine these questions.

Results: We found that the two Australian endemic complex members, Cx. australicus and Cx. globocoxitus, comprise a monophyletic group, are genetically distinct, and are most closely related to the cosmopolitan Cx. quinquefasciatus. Our results also show that Cx. pipiens pallens is genetically distinct, but may have arisen from past hybridization. Lastly, we observed complicated patterns of genetic differentiation within and between Cx. pipiens f. pipiens and Cx. pipiens f. molestus.

Conclusions: Two Australian endemic Culex taxa, Cx. australicus and Cx. globocoxitus, belong within the Cx. pipiens complex, but have a relatively older evolutionary origin. They likely diverged from Cx. quinquefasciatus after its colonization of Australia. The taxon Cx. pipiens pallens is a distinct evolutionary entity that likely arose from past hybridization between Cx. quinquefasciatus and Cx. pipiens f. pipiens/Cx. pipiens f. molestus. Our results do not suggest it derives from ongoing hybridization. Finally, genetic differentiation within the Cx. pipiens f. pipiens and Cx. pipiens f. molestus samples suggests that they collectively form two separate geographic clades, one in North America and one in Europe and the Mediterranean. This may indicate that the Cx. pipiens f. molestus form has two distinct origins, arising from Cx. pipiens f. pipiens in each region. However, ongoing genetic exchange within and between these taxa have obscured their evolutionary histories, and could also explain the absence of monophyly among our samples. Overall, this work suggests many avenues that warrant further investigation.
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http://dx.doi.org/10.1186/s13071-020-3879-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6950815PMC
January 2020

Prosthetic Valve Endocarditis with in a Human European Patient and Its Detection in Red Squirrels ().

J Clin Microbiol 2019 12 23;58(1). Epub 2019 Dec 23.

Department of Medical Microbiology and Hygiene, University of Mainz, Mainz, Germany.

Members of the genus are fastidious Gram-negative facultative intracellular bacteria that are typically transmitted by arthropod vectors. Several spp. have been found to cause culture-negative endocarditis in humans. Here, we report the case of a 75-year-old German woman with prosthetic valve endocarditis due to The infecting agent was characterized by sequencing of six housekeeping genes (16S rRNA, , , , , and ), applying a multilocus sequence typing (MLST) approach. The 5,097 bp of the concatenated housekeeping gene sequence from the patient were 99.0% identical to a sequence from a strain isolated from a red squirrel ( ) from China. A total of 39% (24/62) of red squirrel () samples from the Netherlands were positive for the gene variant detected in the patient. This suggests that the red squirrel is the reservoir host for human infection in Europe.
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http://dx.doi.org/10.1128/JCM.01404-19DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6935924PMC
December 2019

Genetic characterization of Anaplasma phagocytophilum strains from goats (Capra aegagrus hircus) and water buffalo (Bubalus bubalis) by 16S rRNA gene, ankA gene and multilocus sequence typing.

Ticks Tick Borne Dis 2019 10 13;10(6):101267. Epub 2019 Aug 13.

Department of Medical Microbiology and Hygiene, University of Mainz, Obere Zahlbacherstrasse 67, D-55131 Mainz, Germany. Electronic address:

Anaplasma phagocytophilum is a Gram-negative obligate intracellular bacterium that replicates in neutrophil granulocytes. It is transmitted by ticks and causes tick-borne fever in domestic ruminants such as sheep, cattle and goats. However, in contrast to sheep and cattle little is known about the clinical course of infection in goats. We report here on three cases of symptomatic infection with A. phagocytophilum in two goats (Capra aegagrus hircus) and one water buffalo (Bubalus bubalis). The animals showed symptoms and laboratory findings similar to sheep and cattle. To our knowledge, this is the first report on the symptomatic infection of water buffalos with A. phagocytophilum. The infecting strains were genetically characterized by 16S rRNA gene, ankA gene and multilocus sequence typing (MLST). Four other strains from asymptomatically infected goats were also included. The ankA sequences from five goats were part of the formerly described ankA gene clusters I and IV that are known to contain A. phagocytophilum strains from sheep and cattle. However, the sequences from one goat and from the water buffalo belonged to ankA gene cluster II that was formerly described to be restricted to roe deer. A similar observation was made for MLST as three goats clustered with sequences from sheep and cattle, whereas three other goats and the water buffalo were found to be part of the roe deer cluster. However, since most of the strains from sheep and cattle were distinct from the roe deer strains, roe deer might not represent major reservoir hosts for tick-borne fever in domestic ruminants. When differing parts of the 16S rRNA gene were used for typing the results were conflicting. This shows that the use of a standardized typing method such as MLST is highly desirable to generate easily comparable results.
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http://dx.doi.org/10.1016/j.ttbdis.2019.101267DOI Listing
October 2019

Exploring Chihuahuan Desert diversification in the gray-banded kingsnake, Lampropeltis alterna (Serpentes: Colubridae).

Mol Phylogenet Evol 2019 02 31;131:211-218. Epub 2018 Oct 31.

Department of Herpetology, The American Museum of Natural History, Central Park West and 79(th) Street, New York, NY 10024, USA.

Within many biomes, the cause of phylogeographic structure remains unknown even across regions throughout North America, including within the biodiverse Chihuahuan Desert. For example, little is known about population structure or the timing of diversification of Chihuahuan endemics. This is due largely to the lack of population genomic studies within this region. We generated ultra-conserved element data for the gray-banded kingsnake (Lampropeltis alterna) to investigate lineage divergence and historical demography across the Chihuahuan Desert. We found three unique lineages corresponding to the Trans-Pecos and Mapimian biogeographic regions of the Chihuahuan Desert, and a distinct population in the Sierra Madre Occidental. Using several mutation rates to calibrate the timing of divergence among these lineages, we show that lineage divergence likely occurred during the Pleistocene, which indicates that careful consideration needs to be used when applying mutation rates to ultra-conserved elements. We suggest that biogeographic provinces within the Chihuahuan Desert may have served as allopatric refugia during climatic fluctuations of the Quaternary. This work serves as an important template for further testing biogeographic hypotheses within the region.
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http://dx.doi.org/10.1016/j.ympev.2018.10.031DOI Listing
February 2019

Activity of Genes with Functions in Human Williams-Beuren Syndrome Is Impacted by Mobile Element Insertions in the Gray Wolf Genome.

Genome Biol Evol 2018 06;10(6):1546-1553

Department of Biostatistics, UCLA Fielding School of Public Health, Los Angeles, California.

In canines, transposon dynamics have been associated with a hyper-social behavioral syndrome, although the functional mechanism has yet to be described. We investigate the epigenetic and transcriptional consequences of these behavior-associated mobile element insertions (MEIs) in dogs and Yellowstone gray wolves. We posit that the transposons themselves may not be the causative feature; rather, their transcriptional regulation may exert the functional impact. We survey four outlier transposons associated with hyper-sociability, with the expectation that they are targeted for epigenetic silencing. We predict hyper-methylation of MEIs, suggestive that the epigenetic silencing of and not the MEIs themselves may be driving dysregulation of nearby genes. We found that transposon-derived sequences are significantly hyper-methylated, regardless of their copy number or species. Further, we have assessed transcriptome sequence data and found evidence that MEIs impact the expression levels of six genes (WBSCR17, LIMK1, GTF2I, WBSCR27, BAZ1B, and BCL7B), all of which have known roles in human Williams-Beuren syndrome due to changes in copy number, typically hemizygosity. Although further evidence is needed, our results suggest that a few insertions alter local expression at multiple genes, likely through a cis-regulatory mechanism that excludes proximal methylation.
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http://dx.doi.org/10.1093/gbe/evy112DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6007319PMC
June 2018

Sexual Dimorphism and Retinal Mosaic Diversification following the Evolution of a Violet Receptor in Butterflies.

Mol Biol Evol 2017 09;34(9):2271-2284

Department of Ecology and Evolutionary Biology, University of California, Irvine, CA.

Numerous animal lineages have expanded and diversified the opsin-based photoreceptors in their eyes underlying color vision behavior. However, the selective pressures giving rise to new photoreceptors and their spectral tuning remain mostly obscure. Previously, we identified a violet receptor (UV2) that is the result of a UV opsin gene duplication specific to Heliconius butterflies. At the same time the violet receptor evolved, Heliconius evolved UV-yellow coloration on their wings, due to the pigment 3-hydroxykynurenine (3-OHK) and the nanostructure architecture of the scale cells. In order to better understand the selective pressures giving rise to the violet receptor, we characterized opsin expression patterns using immunostaining (14 species) and RNA-Seq (18 species), and reconstructed evolutionary histories of visual traits in five major lineages within Heliconius and one species from the genus Eueides. Opsin expression patterns are hyperdiverse within Heliconius. We identified six unique retinal mosaics and three distinct forms of sexual dimorphism based on ommatidial types within the genus Heliconius. Additionally, phylogenetic analysis revealed independent losses of opsin expression, pseudogenization events, and relaxation of selection on UVRh2 in one lineage. Despite this diversity, the newly evolved violet receptor is retained across most species and sexes surveyed. Discriminability modeling of behaviorally preferred 3-OHK yellow wing coloration suggests that the violet receptor may facilitate Heliconius color vision in the context of conspecific recognition. Our observations give insights into the selective pressures underlying the origins of new visual receptors.
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http://dx.doi.org/10.1093/molbev/msx163DOI Listing
September 2017

The role of latitudinal, genetic and temperature variation in the induction of diapause of Papilio glaucus (Lepidoptera: Papilionidae).

Insect Sci 2018 Apr 21;25(2):328-336. Epub 2017 Feb 21.

Department of Entomology, Michigan State University, East Lansing, Michigan, USA.

A key adaptation in insects for dealing with variable environmental conditions is the ability to diapause. The tiger swallowtail butterflies, Papilio glaucus and P. canadensis are ideal species to explore the genetic causes and population genetic consequences of diapause because divergence in this trait is believed to be a salient factor in maintaining a hybrid zone between these species. Yet little is known about the factors that influence diapause induction in this system. Here we explored how spatial (latitudinal), environmental (temperature) and genetic (hybridization) factors affect diapause induction in this system. Specifically, a series of growth chamber experiments using wild caught individuals from across the eastern United States were performed to: (1) evaluate how critical photoperiod varies with latitude, (2) isolate the stage in which induction occurs, (3) test whether changes in temperature affected rates of diapause induction, and (4) explore how the incidence of diapause is affected in hybrid offspring. We find that induction occurs in the larval stage, is not sensitive to a relatively broad range of temperatures, appears to have a complex genetic basis (i.e., is not simply a dominant trait following a Mendelian inheritance pattern) and that the critical photoperiod increases by 0.4 h with each increasing degree in latitude. This work deepens our understanding of how spatial, environmental and genetic variation influences a key seasonal adaptation (diapause induction) in a well-developed ecological model system and will make possible future studies that explore how climatic variation affects the population dynamics and genetics of this system.
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http://dx.doi.org/10.1111/1744-7917.12423DOI Listing
April 2018

Phylogenetic incongruence and the evolutionary origins of cardenolide-resistant forms of Na(+) ,K(+) -ATPase in Danaus butterflies.

Evolution 2016 08 27;70(8):1913-21. Epub 2016 Jul 27.

Department of Ecology and Evolutionary Biology, Princeton University, Princeton, New Jersey, 08544.

Many distantly related insect species are specialized feeders of cardenolide-containing host plants such as milkweed (Asclepias spp.). Previous studies have revealed frequent, parallel substitution of a functionally important amino acid substitution (N122H) in the alpha subunit of Na(+) ,K(+) -ATPase in a number of these species. This substitution facilitates the ability of these insects to feed on their toxic hosts and sequester cardenolides for their own use in defense. Among milkweed butterflies of the genus Danaus, the previously established phylogeny for this group suggests that N122H arose independently and fixed in two distinct lineages. We reevaluate this conclusion by examining Danaus phylogenetic relationships using >400 orthologous gene sequences assembled from transcriptome data. Our results indicate that the three Danaus species known to harbor the N122H substitution are more closely related than previously thought, consistent with a single, common origin for N122H. However, we also find evidence of both incomplete lineage sorting and post-speciation genetic exchange among these butterfly species, raising the possibility of collateral evolution of cardenolide-insensitivity in this species group.
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http://dx.doi.org/10.1111/evo.12999DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4980202PMC
August 2016

Varying influences of selection and demography in host-adapted populations of the tick-transmitted bacterium, Anaplasma phagocytophilum.

BMC Evol Biol 2015 Mar 31;15:58. Epub 2015 Mar 31.

Department of Medical Microbiology and Hygiene, University of Mainz, Medical Centre, Mainz, Germany.

Background: The host range of a pathogenic bacterial strain likely influences its effective population size, which in turn affects the efficacy of selection. Transmission between competent hosts may occur more frequently for host generalists than for specialists. This could allow higher bacterial population densities to persist within an ecological community and increase the efficacy of selection in these populations. Conversely, specialist strains may be better adapted to their hosts and consequently achieve greater within-host population densities, with corresponding increases in selection efficacy. To assess these different hypotheses, we examined the effective population sizes of three strains of the bacterium Anaplasma phagocytophilum and categorized the varying roles of selection and demography on patterns of genetic diversity and divergence in these populations. A. phagocytophilum is a tick-transmitted, obligately intracellular pathogen. Strains of A. phagocytophilum display varying degrees of host specialization, making this a good species for exploring questions regarding host range, effective population size and selection efficacy.

Results: We found that a roe deer specialist harbored the most genetic diversity of the three A. phagocytophilum strains and correspondingly had the largest effective population size. Another strain that is ecologically specialized on rodents and insectivores had the smallest effective population size. However, these mammalian hosts are distantly related evolutionarily. The third strain, a host generalist, was intermediate in its effective population size between the other two strains. Evolutionary constraint on non-synonymous sites was pervasive in all three strains, although some slightly deleterious mutations may also be segregating in these populations. We additionally found evidence of genome-wide selective sweeps in the generalist strain, whereas signals of repeated bottlenecks were detected in the strain with the smallest effective population size.

Conclusions: A. phagocytophilum is a diverse bacterial species that differs among distinct strains in its effective population size, as well as how genetic diversity and divergence have been influenced by selection and demographic changes. In this species, host specialization may facilitate increased population growth and allow more opportunities for selection to act. These results provide insights into how host range has influenced evolutionary patterns of strain divergence in an emerging zoonotic bacterium.
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http://dx.doi.org/10.1186/s12862-015-0335-zDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4383208PMC
March 2015

Analysis of the population structure of Anaplasma phagocytophilum using multilocus sequence typing.

PLoS One 2014 3;9(4):e93725. Epub 2014 Apr 3.

Institute of Medical Microbiology and Hygiene, University of Freiburg, Freiburg, Germany.

Anaplasma phagocytophilum is a Gram-negative obligate intracellular bacterium that replicates in neutrophils. It is transmitted via tick-bite and causes febrile disease in humans and animals. Human granulocytic anaplasmosis is regarded as an emerging infectious disease in North America, Europe and Asia. However, although increasingly detected, it is still rare in Europe. Clinically apparent A. phagocytophilum infections in animals are mainly found in horses, dogs, cats, sheep and cattle. Evidence from cross-infection experiments that A. phagocytophilum isolates of distinct host origin are not uniformly infectious for heterologous hosts has led to several approaches of molecular strain characterization. Unfortunately, the results of these studies are not always easily comparable, because different gene regions and fragment lengths were investigated. Multilocus sequence typing is a widely accepted method for molecular characterization of bacteria. We here provide for the first time a universal typing method that is easily transferable between different laboratories. We validated our approach on an unprecedented large data set of almost 400 A. phagocytophilum strains from humans and animals mostly from Europe. The typability was 74% (284/383). One major clonal complex containing 177 strains was detected. However, 54% (49/90) of the sequence types were not part of a clonal complex indicating that the population structure of A. phagocytophilum is probably semiclonal. All strains from humans, dogs and horses from Europe belonged to the same clonal complex. As canine and equine granulocytic anaplasmosis occurs frequently in Europe, human granulocytic anaplasmosis is likely to be underdiagnosed in Europe. Further, wild boars and hedgehogs may serve as reservoir hosts of the disease in humans and domestic animals in Europe, because their strains belonged to the same clonal complex. In contrast, as they were only distantly related, roe deer, voles and shrews are unlikely to harbor A. phagocytophilum strains infectious for humans, domestic or farm animals.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0093725PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3974813PMC
January 2015

Parallel molecular evolution in an herbivore community.

Science 2012 Sep;337(6102):1634-7

Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ 08544, USA.

Numerous insects have independently evolved the ability to feed on plants that produce toxic secondary compounds called cardenolides and can sequester these compounds for use in their defense. We surveyed the protein target for cardenolides, the alpha subunit of the sodium pump, Na(+),K(+)-ATPase (ATPα), in 14 species that feed on cardenolide-producing plants and 15 outgroups spanning three insect orders. Despite the large number of potential targets for modulating cardenolide sensitivity, amino acid substitutions associated with host-plant specialization are highly clustered, with many parallel substitutions. Additionally, we document four independent duplications of ATPα with convergent tissue-specific expression patterns. We find that unique substitutions are disproportionately associated with recent duplications relative to parallel substitutions. Together, these findings support the hypothesis that adaptation tends to take evolutionary paths that minimize negative pleiotropy.
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http://dx.doi.org/10.1126/science.1226630DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3770729PMC
September 2012

The evolution of cardenolide-resistant forms of Na⁺,K⁺ -ATPase in Danainae butterflies.

Mol Ecol 2012 Jan 29;21(2):340-9. Epub 2011 Nov 29.

Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ 08544, USA.

Cardenolides are a class of plant secondary compounds that inhibit the proper functioning of the Na(+) , K(+) -ATPase enzyme in susceptible animals. Nonetheless, many insect species are able to sequester cardenolides for their own defence. These include butterflies in the subfamily Danainae (Family: Nymphalidae) such as the monarch (Danaus plexippus). Previous studies demonstrated that monarchs harbour an asparagine (N) to histidine (H) substitution (N122H) in the α subunit of Na(+) , K(+) -ATPase (ATPα) that reduces this enzyme's sensitivity to cardenolides. More recently, it has been suggested that at ATPα position 111, monarchs may also harbour a leucine (L)/glutamine (Q) polymorphism. This later amino acid could also contribute to cardenolide insensitivity. However, here we find that incorrect annotation of the initially reported DNA sequence for ATPα has led to several erroneous conclusions. Using a population genetic and phylogenetic analysis of monarchs and their close relatives, we show that an ancient Q111L substitution occurred prior to the radiation of all Danainae, followed by a second substitution at the same site to valine (V), which arose before the diversification of the Danaus genus. In contrast, N122H appears to be a recent substitution specific to monarchs. Surprisingly, examination of a broader insect phylogeny reveals that the same progression of amino acid substitutions (Q111L → L111V + N122H) has also occurred in Chyrsochus beetles (Family: Chrysomelidae, Subfamily: Eumolpinae) that feed on cardenolide-containing host plants. The parallel pattern of amino acid substitution in these two distantly related lineages is consistent with an adaptive role for these substitutions in reducing cardenolide sensitivity and suggests that their temporal order may be limited by epistatic interactions.
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http://dx.doi.org/10.1111/j.1365-294X.2011.05379.xDOI Listing
January 2012

Sex chromosome mosaicism and hybrid speciation among tiger swallowtail butterflies.

PLoS Genet 2011 Sep 8;7(9):e1002274. Epub 2011 Sep 8.

Section of Integrative Biology, University of Texas, Austin, Texas, United States of America.

Hybrid speciation, or the formation of a daughter species due to interbreeding between two parental species, is a potentially important means of diversification, because it generates new forms from existing variation. However, factors responsible for the origin and maintenance of hybrid species are largely unknown. Here we show that the North American butterfly Papilio appalachiensis is a hybrid species, with genomic admixture from Papilio glaucus and Papilio canadensis. Papilio appalachiensis has a mosaic phenotype, which is hypothesized to be the result of combining sex-linked traits from P. glaucus and P. canadensis. We show that P. appalachiensis' Z-linked genes associated with a cooler thermal habitat were inherited from P. canadensis, whereas its W-linked mimicry and mitochondrial DNA were inherited from P. glaucus. Furthermore, genome-wide AFLP markers showed nearly equal contributions from each parental species in the origin of P. appalachiensis, indicating that it formed from a burst of hybridization between the parental species, with little subsequent backcrossing. However, analyses of genetic differentiation, clustering, and polymorphism based on molecular data also showed that P. appalachiensis is genetically distinct from both parental species. Population genetic simulations revealed P. appalachiensis to be much younger than the parental species, with unidirectional gene flow from P. glaucus and P. canadensis into P. appalachiensis. Finally, phylogenetic analyses, combined with ancestral state reconstruction, showed that the two traits that define P. appalachiensis' mosaic phenotype, obligatory pupal diapause and mimicry, evolved uniquely in P. canadensis and P. glaucus, respectively, and were then recombined through hybridization to form P. appalachiensis. These results suggest that natural selection and sex-linked traits may have played an important role in the origin and maintenance of P. appalachiensis as a hybrid species. In particular, ecological barriers associated with a steep thermal cline appear to maintain the distinct, mosaic genome of P. appalachiensis despite contact and occasional hybridization with both parental species.
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http://dx.doi.org/10.1371/journal.pgen.1002274DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3169544PMC
September 2011

Allochronic isolation and incipient hybrid speciation in tiger swallowtail butterflies.

Oecologia 2010 Feb 24;162(2):523-31. Epub 2009 Nov 24.

Department of Entomology, Michigan State University, 243 Natural Sciences Building, East Lansing, MI 48824, USA.

Hybridization leading to reproductively isolated, novel genotypes is poorly understood as a means of speciation and few empirical examples have been studied. In 1999, a previously non-existent delayed flight of what appeared to be the Canadian tiger swallowtail butterfly, Papilio canadensis, was observed in the Battenkill River Valley, USA. Allozyme frequencies and morphology suggest that this delayed flight was the product of hybridization between Papilio canadensis and its sibling species Papilio glaucus. The mitochondrial DNA (mtDNA) restriction fragment length polymorphisms presented here indicate that only P. canadensis-like mtDNA occurs in this population, suggesting that introgression likely occurred from hybrid males mating with P. canadensis females. Preliminary studies of this population indicated that delayed post-diapause pupal emergence in this hybrid genotype was the root cause behind the observed delayed flight, which suggests a potential empirical example of a mechanism leading to reproductive isolation. Here we provide further evidence of the role of adult pupal emergence as a reproductive barrier likely leading to reproductive isolation. In particular, we present results from pupal emergence studies using four different spring and two different winter temperature treatments. The results indicate a clear separation of adult emergences between the hybrid population and both parental species. However, our results indicate that exceptionally hot springs are likely to lead to greater potential for overlap between the local parental species, P. canadensis, and this delayed population with hybrid origins. Conversely, our results also show that warmer winters are likely to increase the temporal separation of the hybrid population and the parental species. Finally, we report recently collected evidence that this hybrid population remains morphologically distinct.
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http://dx.doi.org/10.1007/s00442-009-1493-8DOI Listing
February 2010
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