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USGS2013

White-nose syndrome in bats: Illuminating the darkness

Happy ten-year anniversary to BMC Biology! We can attest to the effectiveness of the journal in reaching a great diversity of scientists based on reader responses to our commentary [1] about bat white-nose syndrome (WNS) two years ago. WNS is still on course to rank among the most destructive wildlife diseases to emerge in recent history, and it has continued to have unprecedented effects on populations of hibernating bats in eastern North America. At the time of our last writing in November 2010, the cold-adapted fungus then presumed to cause WNS ( Geomyces destructans ) had spread about 1,300 km from an index site in New York (Figure 1). In those early years of the epizootic, WNS caused a staggering wave of mass mortality among all six species of hibernating bats that occur in north-eastern North America. Since November 2010, WNS has spread into eight additional US states and two more Canadian provinces (Figure 1), and has continued to cause mortality in those six species most affected during the early years of the epizootic. Although part of a mostly tragic story has continued to unfold as new areas are affected, anecdotal signs are emerging that all may not be lost when it comes to hibernating bats and WNS. Amid the continued large-scale population declines of certain species, we have yet to see mass mortality in some of the more westerly areas where the fungus was detected two winters ago (Figure 1). Also, recently disease without obvious mortality was diagnosed in gray bats ( Myotis grisescens ) - an endangered species thought by many two years ago to be at high risk of extinction from WNS. Clearly, large gaps in our understanding of WNS remain, but some have been filled since we last communicated with readers of BMC Biology.

BMC Biology↗

USGS2010

Wing pathology of white-nose syndrome in bats suggests life-threatening disruption of physiology

White-nose syndrome (WNS) is causing unprecedented declines in several species of North American bats. The characteristic lesions of WNS are caused by the fungus Geomyces destructans , which erodes and replaces the living skin of bats while they hibernate. It is unknown how this infection kills the bats. We review here the unique physiological importance of wings to hibernating bats in relation to the damage caused by G. destructans and propose that mortality is caused by catastrophic disruption of wing-dependent physiological functions. Mechanisms of disease associated with G. destructans seem specific to hibernating bats and are most analogous to disease caused by chytrid fungus in amphibians.

BMC Biology↗

USGS2010

Population structure and plumage polymorphism: the intraspecific evolutionary relationships of a polymorphic raptor, Buteo jamaicensis harlani

Background Phenotypic and molecular genetic data often provide conflicting patterns of intraspecific relationships confounding phylogenetic inference, particularly among birds where a variety of environmental factors may influence plumage characters. Among diurnal raptors, the taxonomic relationship of Buteo jamaicensis harlani to other B. jamaicensis subspecies has been long debated because of the polytypic nature of the plumage characteristics used in subspecies or species designations. Results To address the evolutionary relationships within this group, we used data from 17 nuclear microsatellite loci, 430 base pairs of the mitochondrial control region, and 829 base pairs of the melanocortin 1 receptor ( Mc1r ) to investigate molecular genetic differentiation among three B. jamaicensis subspecies ( B. j. borealis , B. j. calurus , B. j. harlani ). Bayesian clustering analyses of nuclear microsatellite loci showed no significant differences between B. j. harlani and B. j. borealis . Differences observed between B. j. harlani and B. j. borealis in mitochondrial and microsatellite data were equivalent to those found between morphologically similar subspecies, B. j. borealis and B. j. calurus , and estimates of migration rates among all three subspecies were high. No consistent differences were observed in Mc1r data between B. j. harlani and other B. jamaicensis subspecies or between light and dark color morphs within B. j. calurus , suggesting that Mc1r does not play a significant role in B. jamaicensis melanism. Conclusions These data suggest recent interbreeding and gene flow between B. j. harlani and the other B. jamaicensis subspecies examined, providing no support for the historical designation of B. j. harlani as a distinct species.

BMC Evolutionary Biology↗

USGS2014

Distribution and population genetics of walleye and sauger

Conserving genetic diversity and local adaptations are management priorities for wild populations of exploited species, which increasingly are subject to climate change, habitat loss, and pollution. These constitute growing concerns for the walleye Sander vitreus, an ecologically and economically valuable North American temperate fish with large Laurentian Great Lakes' fisheries. This study compares genetic diversity and divergence patterns across its widespread native range using mitochondrial (mt) DNA control region sequences and nine nuclear DNA microsatellite (μsat) loci, examining historic and contemporary influences. We analyze the genetic and morphological characters of a putative endemic variant– “blue pike” S. v. “glaucus” –described from Lakes Erie and Ontario, which became extinct. Walleye with turquoise-colored mucus also are evaluated, since some have questioned whether these are related to the “blue pike”.

BMC Evolutionary Biology↗

USGS2007

Chromosome painting in the manatee supports Afrotheria and Paenungulata

Background Sirenia (manatees, dugongs and Stellar's sea cow) have no evolutionary relationship with other marine mammals, despite similarities in adaptations and body shape. Recent phylogenomic results place Sirenia in Afrotheria and with elephants and rock hyraxes in Paenungulata. Sirenia and Hyracoidea are the two afrotherian orders as yet unstudied by comparative molecular cytogenetics. Here we report on the chromosome painting of the Florida manatee. Results The human autosomal and X chromosome paints delimited a total of 44 homologous segments in the manatee genome. The synteny of nine of the 22 human autosomal chromosomes (4, 5, 6, 9, 11, 14, 17, 18 and 20) and the X chromosome were found intact in the manatee. The syntenies of other human chromosomes were disrupted in the manatee genome into two to five segments. The hybridization pattern revealed that 20 (15 unique) associations of human chromosome segments are found in the manatee genome: 1/15, 1/19, 2/3 (twice), 3/7 (twice), 3/13, 3/21, 5/21, 7/16, 8/22, 10/12 (twice), 11/20, 12/22 (three times), 14/15, 16/19 and 18/19. Conclusion There are five derived chromosome traits that strongly link elephants with manatees in Tethytheria and give implicit support to Paenungulata: the associations 2/3, 3/13, 8/22, 18/19 and the loss of the ancestral eutherian 4/8 association. It would be useful to test these conclusions with chromosome painting in hyraxes. The manatee chromosome painting data confirm that the associations 1/19 and 5/21 phylogenetically link afrotherian species and show that Afrotheria is a natural clade. The association 10/12/22 is also ubiquitous in Afrotheria (clade I), present in Laurasiatheria (clade IV), only partially present in Xenarthra (10/12, clade II) and absent in Euarchontoglires (clade III). If Afrotheria is basal to eutherians, this association could be part of the ancestral eutherian karyotype. If afrotherians are not at the root of the eutherian tree, then the 10/12/22 association could be one of a suite of derived associations linking afrotherian taxa.

BMC Evolutionary Biology↗

USGS2008

Tracing the first steps of American sturgeon pioneers in Europe

Background. A Baltic population of Atlantic sturgeon was founded ???1,200 years ago by migrants from North America, but after centuries of persistence, the population was extirpated in the 1960s, mainly as a result of over-harvest and habitat alterations. As there are four genetically distinct groups of Atlantic sturgeon inhabiting North American rivers today, we investigated the genetic provenance of the historic Baltic population by ancient DNA analyses using mitochondrial and nuclear markers. Results. The phylogeographic signal obtained from multilocus microsatellite DNA genotypes and mitochondrial DNA control region haplotypes, when compared to existing baseline datasets from extant populations, allowed for the identification of the region-of-origin of the North American Atlantic sturgeon founders. Moreover, statistical and simulation analyses of the multilocus genotypes allowed for the calculation of the effective number of individuals that originally founded the European population of Atlantic sturgeon. Our findings suggest that the Baltic population of A. oxyrinchus descended from a relatively small number of founders originating from the northern extent of the species' range in North America. Conclusion. These results demonstrate that the most northerly distributed North American A. oxyrinchus colonized the Baltic Sea ???1,200 years ago, suggesting that Canadian specimens should be the primary source of broodstock used for restoration in Baltic rivers. This study illustrates the great potential of patterns obtained from ancient DNA to identify population-of-origin to investigate historic genotype structure of extinct populations. ?? 2008 Ludwig et al; licensee BioMed Central Ltd.

BMC Evolutionary Biology↗

USGS2008

Genetic structure along an elevational gradient in Hawaiian honeycreepers reveals contrasting evolutionary responses to avian malaria

Background. The Hawaiian honeycreepers (Drepanidinae) are one of the best-known examples of an adaptive radiation, but their persistence today is threatened by the introduction of exotic pathogens and their vector, the mosquito Culex quinquefasciatus. Historically, species such as the amakihi (Hemignathus virens), the apapane (Himatione sanguinea), and the iiwi (Vestiaria coccinea) were found from the coastal lowlands to the high elevation forests, but by the late 1800's they had become extremely rare in habitats below 900 m. Recently, however, populations of amakihi and apapane have been observed in low elevation habitats. We used twelve polymorphic microsatellite loci to investigate patterns of genetic structure, and to infer responses of these species to introduced avian malaria along an elevational gradient on the eastern flanks of Mauna Loa and Kilauea volcanoes on the island of Hawaii. Results. Our results indicate that amakihi have genetically distinct, spatially structured populations that correspond with altitude. We detected very few apapane and no iiwi in low-elevation habitats, and genetic results reveal only minimal differentiation between populations at different altitudes in either of these species. Conclusion. Our results suggest that amakihi populations in low elevation habitats have not been recolonized by individuals from mid or high elevation refuges. After generations of strong selection for pathogen resistance, these populations have rebounded and amakihi have become common in regions in which they were previously rare or absent. ?? 2008 Eggert et al; licensee BioMed Central Ltd.

BMC Evolutionary Biology↗

USGS2009

Evidence that pairing with genetically similar mates is maladaptive in a monogamous bird

Background Evidence of multiple genetic criteria of mate choice is accumulating in numerous taxa. In many species, females have been shown to pair with genetically dissimilar mates or with extra-pair partners that are more genetically compatible than their social mates, thereby increasing their offsprings' heterozygosity which often correlates with offspring fitness. While most studies have focused on genetically promiscuous species, few studies have addressed genetically monogamous species, in which mate choice tends to be mutual. Results Here, we used microsatellite markers to assess individual global heterozygosity and genetic similarity of pairs in a socially and genetically monogamous seabird, the black-legged kittiwake Rissa tridactyla . We found that pairs were more genetically dissimilar than expected by chance. We also identified fitness costs of breeding with genetically similar partners: (i) genetic similarity of pairs was negatively correlated with the number of chicks hatched, and (ii) offspring heterozygosity was positively correlated with growth rate and survival. Conclusion These findings provide evidence that breeders in a genetically monogamous species may avoid the fitness costs of reproducing with a genetically similar mate. In such species that lack the opportunity to obtain extra-pair fertilizations, mate choice may therefore be under high selective pressure.

Alaska↗

USGS2016

Genetic and phenotypic variation along an ecological gradient in lake trout Salvelinus namaycush

Background Adaptive radiation involving a colonizing phenotype that rapidly evolves into at least one other ecological variant, or ecotype, has been observed in a variety of freshwater fishes in post-glacial environments. However, few studies consider how phenotypic traits vary with regard to neutral genetic partitioning along ecological gradients. Here, we present the first detailed investigation of lake trout Salvelinus namaycush that considers variation as a cline rather than discriminatory among ecotypes. Genetic and phenotypic traits organized along common ecological gradients of water depth and geographic distance provide important insights into diversification processes in a lake with high levels of human disturbance from over-fishing. Results Four putative lake trout ecotypes could not be distinguished using population genetic methods, despite morphological differences. Neutral genetic partitioning in lake trout was stronger along a gradient of water depth, than by locality or ecotype. Contemporary genetic migration patterns were consistent with isolation-by-depth. Historical gene flow patterns indicated colonization from shallow to deep water. Comparison of phenotypic ( Pst ) and neutral genetic variation ( Fst ) revealed that morphological traits related to swimming performance (e.g., buoyancy, pelvic fin length) departed more strongly from neutral expectations along a depth gradient than craniofacial feeding traits. Elevated phenotypic variance with increasing water depth in pelvic fin length indicated possible ongoing character release and diversification. Finally, differences in early growth rate and asymptotic fish length across depth strata may be associated with limiting factors attributable to cold deep-water environments. Conclusion We provide evidence of reductions in gene flow and divergent natural selection associated with water depth in Lake Superior. Such information is relevant for documenting intraspecific biodiversity in the largest freshwater lake in the world for a species that recently lost considerable genetic diversity and is now in recovery. Unknown is whether observed patterns are a result of an early stage of incipient speciation, gene flow-selection equilibrium, or reverse speciation causing formerly divergent ecotypes to collapse into a single gene pool.

Lake Superior, Isle Royale↗

USGS2019

Global phylodynamic analysis of avian paramyxovirus-1 provides evidence of inter-host transmission and intercontinental spatial diffusion

Background Avian avulavirus (commonly known as avian paramyxovirus-1 or APMV-1) can cause disease of varying severity in both domestic and wild birds. Understanding how viruses move among hosts and geography would be useful for informing prevention and control efforts. A Bayesian statistical framework was employed to estimate the evolutionary history of 1602 complete fusion gene APMV-1 sequences collected from 1970 to 2016 in order to infer viral transmission between avian host orders and diffusion among geographic regions. Ancestral states were estimated with a non-reversible continuous-time Markov chain model, allowing transition rates between discrete states to be calculated. The evolutionary analyses were stratified by APMV-1 classes I ( n = 198) and II ( n = 1404), and only those sequences collected between 2006 and 2016 were allowed to contribute host and location information to the viral migration networks. Results While the current data was unable to assess impact of host domestication status on APMV-1 diffusion, these analyses supported the sharing of APMV-1 among divergent host taxa. The highest supported transition rate for both classes existed from domestic chickens to Anseriformes (class I:6.18 transitions/year, 95% highest posterior density (HPD) 0.31–20.02, Bayes factor (BF) = 367.2; class II:2.88 transitions/year, 95%HPD 1.9–4.06, BF = 34,582.9). Further, among class II viruses, domestic chickens also acted as a source for Columbiformes (BF = 34,582.9), other Galliformes (BF = 34,582.9), and Psittaciformes (BF = 34,582.9). Columbiformes was also a highly supported source to Anseriformes (BF = 322.0) and domestic chickens (BF = 402.6). Additionally, our results provide support for the diffusion of viruses among continents and regions, but no interhemispheric viral exchange between 2006 and 2016. Among class II viruses, the highest transition rates were estimated from South Asia to the Middle East (1.21 transitions/year; 95%HPD 0.36–2.45; BF = 67,107.8), from Europe to East Asia (1.17 transitions/year; 95%HPD 0.12–2.61; BF = 436.2) and from Europe to Africa (1.06 transitions/year, 95%HPD 0.07–2.51; BF = 169.3). Conclusions While migration appears to occur infrequently, geographic movement may be important in determining viral diversification and population structure. In contrast, inter-order transmission of APMV-1 may occur readily, but most events are transient with few lineages persisting in novel hosts.

BMC Evolutionary Biology↗

USGS2013

Custom microarray construction and analysis for determining potential biomarkers of subchronic androgen exposure in the Eastern Mosquitofish ( Gambusia holbrooki )

Background The eastern mosquitofish ( Gambusia holbrooki ) has the potential to become a bioindicator organism of endocrine disrupting chemicals (EDCs) due to its androgen-driven secondary sexual characteristics. However, the lack of molecular information on G . holbrooki hinders its use as a bioindicator coupled with biomarker data. While traditional gene-by-gene approaches provide insight for biomarker development, a holistic analysis would provide more rapid and expansive determination of potential biomarkers. The objective of this study was to develop and utilize a mosquitofish microarray to determine potential biomarkers of subchronic androgen exposure. To achieve this objective, two specific aims were developed: 1) Sequence a G . holbrooki cDNA library, and 2) Use microarray analysis to determine genes that are differentially regulated by subchronic androgen exposure in hepatic tissues of 17β-trenbolone (TB) exposed adult female G . holbrooki . Results A normalized library of multiple organs of male and female G . holbrooki was prepared and sequenced by the Illumina GA IIx and Roche 454 XLR70. Over 30,000 genes with e-value ≤ 10 -4 were annotated and 14,758 of these genes were selected for inclusion on the microarray. Hepatic microarray analysis of adult female G . holbrooki exposed to the vehicle control or 1 μg/L of TB (a potent anabolic androgen) revealed 229 genes upregulated and 279 downregulated by TB (one-way ANOVA, p < 0.05, FDR α = 0.05, fold change > 1.5 and < −1.5). Fifteen gene ontology biological processes were enriched by TB exposure (Fisher’s Exact Test, p < 0.05). The expression levels of 17β - hydroxysteroid dehydrogenase 3 and zona pellucida glycoprotein 2 were validated by quantitative polymerase chain reaction (qPCR) (Student’s t-test, p < 0.05). Conclusions Coupling microarray data with phenotypic changes driven by androgen exposure in mosquitofish is key for developing this organism into a bioindicator for EDCs. Future studies using this array will enhance knowledge of the biology and toxicological response of this species. This work provides a foundation of molecular knowledge and tools that can be used to delve further into understanding the biology of G . holbrooki and how this organism can be used as a bioindicator organism for endocrine disrupting pollutants in the environment.

BMC Genomics↗