Article

Signatures of natural and unnatural selection: evidence from an immune system gene in African buffalo

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Abstract

Pathogens often have negative effects on wildlife populations, and disease management strategies are important for mitigating opportunities for pathogen transmission. Bovine tuberculosis (Mycobacterium bovis; BTB) is widespread among African buffalo (Syncerus caffer) populations in southern Africa, and strategies for managing this disease vary. In two high profile parks, Kruger National Park (KNP) and Hluhluwe-iMfolozi Park (HIP), BTB is either not actively managed (KNP) or managed using a test-and-cull program (HIP). Exploiting this variation in management tactics, we investigated potential evolutionary consequences of BTB and BTB management on buffalo by examining genetic diversity at IFNG, a locus which codes for interferon gamma, a signaling molecule vital in the immune response to BTB. Both heterozygosity and allelic richness were significantly and positively correlated with chromosomal distance from IFNG in KNP, suggesting that directional selection is acting on IFNG among buffalo in this park. While we did not see the same reduction in genetic variation around IFNG in HIP, we found evidence of a recent bottleneck, which might have eroded this signature due to genome-wide reductions in diversity. In KNP, alleles at IFNG were in significant gametic disequilibrium at both short and long chromosomal distances, but no statistically significant gametic disequilibrium was associated with IFNG in HIP. When, we compared genetic diversity between culled and non-culled subsets of HIP animals, we also found that individuals in the culled group had more rare alleles than those in the non-culled group, and that these rare alleles occurred at higher frequency. The observed excess of rare alleles in culled buffalo and the patterns of gametic disequilibrium in HIP suggest that management may be eroding immunogenetic diversity, disrupting haplotype associations in this population. Taken together, our results suggest that both infectious diseases and disease management strategies can influence host genetic diversity with important evolutionary consequences.

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... Although selective sweeps are generally observed with directional selection, they can also occur during the early phase of balancing selection [67]. In a recent study in KNP and HiP, decreased H e at neighbouring loci BMS1617 and IFNG relative to other nearby loci has been attributed to a selective sweep, providing additional support for this scenario [68]. The relatively low microsatellite H e in southern Africa is unlikely to be caused by low effective population size considering the correlation between short-term hitchhiking effects in southern KNP and long-term hitchhiking effects across Africa, and considering that mtDNA nucleotide diversity (π) is actually considerably higher in southern Africa than in East Africa (D-loop: 0.047 vs. 0.036; complete mitogenome: 0.0048 vs. 0.0035) [69,70]. ...
... Mb at three locus pairs (six loci) in a 34 Mb region, occurring on chromosome 5 in cattle (D' = 0.28-0.43; i.e., LD is at 28-43% of its maximum possible value) [54,68]. The observation of long-distance LD in KNP at chromosomal distances � 5.9 Mb is surprising, especially considering that high haploid and autosomal diversity indicate a large historical effective population size for the KNP buffalo (34 mitochondrial D-loop haplotypes with gene diversity H = 0.94; 15 Y-chromosomal haplotypes with H = 0.74; whole-genome sequencing: high genome-wide observed heterozygosity compared to other mammals: H = 0.00324, low median inbreeding coefficient: f = 0.00060) [21,24,71,78]. ...
... In gray wolf (Canus lupus) and coyote (Canus latrans) LD extends to a distance of~5 Mb, even in small or bottlenecked populations apart from the wolf population of Isle Royale, which consisted of just 10-30 individuals [79][80][81][82][83][84]. Further, the half-length of LD (the distance at which LD is 50% of its maximal value) in two isolated Canadian populations of bighorn sheep (Ovis canadensis) is only 25%-40% of that in KNP buffalo, despite their small size of less than 200 individuals each (4.6-7.5 Mb vs.~20 Mb at chromosome 5 in buffalo) [68,85,86]. ...
Article
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A high genetic load can negatively affect population viability and increase susceptibility to diseases and other environmental stressors. Prior microsatellite studies of two African buffalo ( Syncerus caffer ) populations in South Africa indicated substantial genome-wide genetic load due to high-frequency occurrence of deleterious alleles. The occurrence of these alleles, which negatively affect male body condition and bovine tuberculosis resistance, throughout most of the buffalo’s range were evaluated in this study. Using available microsatellite data (2–17 microsatellite loci) for 1676 animals from 34 localities (from 25°S to 5°N), we uncovered continent-wide frequency clines of microsatellite alleles associated with the aforementioned male traits. Frequencies decreased over a south-to-north latitude range (average per-locus Pearson r = -0.22). The frequency clines coincided with a multilocus-heterozygosity cline (adjusted R ² = 0.84), showing up to a 16% decrease in southern Africa compared to East Africa. Furthermore, continent-wide linkage disequilibrium (LD) at five linked locus pairs was detected, characterized by a high fraction of positive interlocus associations (0.66, 95% CI: 0.53, 0.77) between male-deleterious-trait-associated alleles. Our findings suggest continent-wide and genome-wide selection of male-deleterious alleles driven by an earlier observed sex-chromosomal meiotic drive system, resulting in frequency clines, reduced heterozygosity due to hitchhiking effects and extensive LD due to male-deleterious alleles co-occurring in haplotypes. The selection pressures involved must be high to prevent destruction of allele-frequency clines and haplotypes by LD decay. Since most buffalo populations are stable, these results indicate that natural mammal populations, depending on their genetic background, can withstand a high genetic load.
... DNA was extracted from tissue samples using the Qiagen Blood & Tissue Kit following the manufacturer's protocol. DNA samples were genotyped at the BL4 microsatellite locus, which is located ∼3 cM upstream of the interferon gamma gene (31). BL4 and other microsatellites in this chromsomal region have been associated with nematode resistance in sheep (28,29,55,56). ...
... The BL4 locus has also previously been associated with nematode resistance in African buffalo (30). Genotyping was performed using PCR and fluorescently labeled DNA fragment visualization on an ABI3130xl automated capillary sequencer (Applied Biosystems) as described in ref. 31. Allele sizes were determined using the ABI GS600LIZ ladder (Applied Biosystems). ...
... Chromatograms were analyzed by two independent technicians using Gene-Mapper v3.7. Tests for the presence of null alleles and deviations from Hardy-Weinberg proportions (HWP) showed no null alleles present at BL4 and no deviations from HWP (31). ...
Article
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Pathogen interactions arising during coinfection can exacerbate disease severity, for example when the immune response mounted against one pathogen negatively affects defense of another. It is also possible that host immune responses to a pathogen, shaped by historical evolutionary interactions between host and pathogen, may modify host immune defenses in ways that have repercussions for other pathogens. In this case, negative interactions between two pathogens could emerge even in the absence of concurrent infection. Parasitic worms and tuberculosis (TB) are involved in one of the most geographically extensive of pathogen interactions, and during coinfection worms can exacerbate TB disease outcomes. Here, we show that in a wild mammal natural resistance to worms affects bovine tuberculosis (BTB) severity independently of active worm infection. We found that worm-resistant individuals were more likely to die of BTB than were nonresistant individuals, and their disease progressed more quickly. Anthelmintic treatment moderated, but did not eliminate, the resistance effect, and the effects of resistance and treatment were opposite and additive, with untreated, resistant individuals experiencing the highest mortality. Furthermore, resistance and anthelmintic treatment had nonoverlapping effects on BTB pathology. The effects of resistance manifested in the lungs (the primary site of BTB infection), while the effects of treatment manifested almost entirely in the lymph nodes (the site of disseminated disease), suggesting that resistance and active worm infection affect BTB progression via distinct mechanisms. Our findings reveal that interactions between pathogens can occur as a consequence of processes arising on very different timescales.
... By way of background information, it is worth noting that the HiP buffalo population has the lowest genetic diversity (autosomal DNA, Y-chromosomal DNA and mitochondrial DNA) of any buffalo population studied so far [6,[17][18][19], except for the small South African populations of St. Lucia and Addo (< 200 animals) [20]. Low genetic diversity can probably largely be attributed to a founder event, which is supported by microsatellite-based bottleneck tests [21]. The HiP buffalo population has been completely isolated for about 100 years and was founded by only a few individuals in 1895, increasing to 75 at most in 1929 [17]. ...
... The HiP buffalo population has been completely isolated for about 100 years and was founded by only a few individuals in 1895, increasing to 75 at most in 1929 [17]. Population size remained below 800 until the mid-1950s, due to wildlife culling in the 1930s and 1940s aimed at eradicating trypanosomiasis [21,22]. Random genetic drift caused by the founder event may by itself explain the relatively low frequencies of the DE and SAE alleles in HiP. ...
... A test-and-cull program was initiated in HiP in 1999 (still ongoing in 2006) in an attempt to eradicate BTB. Buffalo were tested for BTB with only BTB-negative individuals released back into the park [21,24]. The culling was extensive, with 260-950 animals per year tested in a population of no more than 4000 fertility are hypothesized to have a net negative effect on male relative fitness. ...
Article
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Bovine tuberculosis (BTB) is endemic to the African buffalo (Syncerus caffer) of Hluhluwe-iMfolozi Park (HiP) and Kruger National Park, South Africa. In HiP, the disease has been actively managed since 1999 through a test-and-cull procedure targeting BTB-positive buffalo. Prior studies in Kruger showed associations between microsatellite alleles, BTB and body condition. A sex chromosomal meiotic drive, a form of natural gene drive, was hypothesized to be ultimately responsible. These associations indicate high-frequency occurrence of two types of male-deleterious alleles (or multiple-allele haplotypes). One type negatively affects body condition and BTB resistance in both sexes. The other type has sexually antagonistic effects: negative in males but positive in females. Here, we investigate whether a similar gene drive system is present in HiP buffalo, using 17 autosomal microsatellites and microsatellite-derived Y-chromosomal haplotypes from 401 individuals, culled in 2002-2004. We show that the association between autosomal microsatellite alleles and BTB susceptibility detected in Kruger, is also present in HiP. Further, Y-haplotype frequency dynamics indicated that a sex chromosomal meiotic drive also occurred in HiP. BTB was associated with negative selection of male-deleterious alleles in HiP, unlike positive selection in Kruger. Birth sex ratios were female-biased. We attribute negative selection and female-biased sex ratios in HiP to the absence of a Y-chromosomal sex-ratio distorter. This distorter has been hypothesized to contribute to positive selection of male-deleterious alleles and male-biased birth sex ratios in Kruger. As previously shown in Kruger, microsatellite alleles were only associated with male-deleterious effects in individuals born after wet pre-birth years; a phenomenon attributed to epigenetic modification. We identified two additional allele types: male-specific deleterious and beneficial alleles, with no discernible effect on females. Finally, we discuss how our findings may be used for breeding disease-free buffalo and implementing BTB test-and-cull programs.
... The fourth pair consists of microsatellites ILSTS026 and INRA006 , which are probably˜18 Mb apart on the same chromosome in buffalo. This chromosome corresponds to a fusing of chromosomes 2 and 3 in cattle, with the former harbouring ILSTS026 and the latterINRA006 , in both cases˜9.5 Mb from the end of the left-side of their p arms (Text S4) (Gallagher & Womack, 1992;Goudet, , 2001Ihara et al., 2004;Lane-deGraaf et al., 2015;Liu & Muse, 2005;Weng, Saatchi, Schnabel, Taylor, & Garrick, 2014). Two additional microsatellite pairs are at close chromosomal distance, although they did not show significant LD in KNP or HiP:INRA006 -TGLA263 (27.5 Mb in buffalo, chromosome 3 in cattle) and TGLA057 -INRA128 (28.3 Mb, chromosome 1) (Ihara et al., 2004). ...
... Long-distance LD appears to occur genome-wide considering that significant LD has also been observed in KNP for theINFNG -GLYCAM1 locus pair, which has an interlocus distance of 18 Mb and occurs on chromosome 5 in cattle (D ' = 0.28, i.e. LD is at 28% of its maximum possible value) (Ihara et al., 2004;Lane-deGraaf et al., 2015). This is a relatively large distance, especially considering that high haploid diversity indicates a large effective population size for the KNP buffalo (34 mitochondrial D-loop haplotypes with H (gene diversity) = 0.94, 15 Y-chromosomal haplotypes with H = 0.74; census sizẽ 37,000 in 2010) (Greyling, 2007;van Hooft et al., 2018;van Hooft et al., 2007). ...
... This process can result in an evolutionary rescue of a species (Carlson et al. 2014;Maslo and Fefferman 2015), where disease-resistant animals increase in number subsequent to initial population declines from strong selective sweeps from disease. Supporting this would be scans of immune genes showing signatures consistent with selection in buffalo (Lane-deGraaf et al. 2015) and more broadly ungulates (Schaschl et al. 2006). The prion gene (PRNP) is of particular relevance for screening in cervids because of its link to chronic wasting disease resistance. ...
Chapter
Humans have long relied on ungulates for food, clothing, manual labor, and transportation. Ungulates were among the first species to be domesticated and managed in the wild, but more than one-third of species are currently of conservation concern. Starting in the late twentieth century, ungulate research and management began employing genetic tools to assess attributes like the degree of population structure, inbreeding, and variation in functionally important genes. As sequencing technology advanced, research on ungulates shifted to now assay variation across the entire genome. More than 20 ungulates have had their genome assembled with a mean length of 2.6 Gb and N50 of 26 Mb. Genomic studies have provided deeper insights into the evolutionary relationships among giraffes and bovids, while camelids and horses have had their entire species demographic histories reconstructed using novel Markovian coalescent models. Moreover, artificial and natural selection has left clear signatures on ungulate genomes with high-throughput sequencing techniques being used to identify the genetic basis to important phenotypic traits. Novel assembly strategies and genomic assays are regularly being employed on ungulates, and research on this ecological and economically valuable group will help chart the course of the emerging field of wildlife genomics.
... Management actions aimed at controlling disease in wildlife populations can sometimes have unintended genetic consequences. For instance, a selective culling program to reduce bTB in African buffalo resulted in a higher frequency of rare alleles at the IFNG locus, which codes for interferon gamma, of crucial importance for immune response, compared to non-culled populations (Lane-deGraaf et al. 2015). This suggests that culling was leading to a loss of immunogenetic diversity, with potentially important evolutionary and future population consequences. ...
Article
Wildlife diseases can have significant impacts on wildlife conservation and management. Many of the pathogens that affect wildlife also have important implications for domestic animal and human health. However, management interventions to prevent or control wildlife disease are hampered by uncertainties about the complex interactions between pathogens and free-ranging wildlife. We often lack crucial knowledge about host ecology, pathogen characteristics, and host-pathogen dynamics. The purpose of this review is to familiarize wildlife biologists and managers with the application of genetic and genomic methodologies for investigating pathogen and host biology to better understand and manage wildlife diseases. The genesis of this review was a symposium at the 2013 annual Wildlife Society Conference. We reviewed the scientific literature and used our personal experiences to identify studies that illustrate the application of genetic and genomic methods to advance our understanding of wildlife epidemiology, focusing on recent research, new techniques, and innovative approaches. Using examples from a variety of pathogen types and a broad array of vertebrate taxa, we describe how genetics and genomics can provide tools to detect and characterize pathogens, uncover routes of disease transmission and spread, shed light on the ways that disease susceptibility is influenced by both host and pathogen attributes, and elucidate the impacts of disease on wildlife populations. Genetic and increasingly genomic methodologies will continue to contribute important insights into pathogen and host biology that will aid efforts to assess and mitigate the impacts of wildlife diseases on global health and conservation of biodiversity.
... Several of these candidate genes were previously reported in other livestock populations (Supporting Information Table S3). For example, EIF3I gene in goats (Sayre, 2010); VPS13B and TEX15 in buffalo (Lane-deGraaf et al., 2015;Liu et al., 2018); GPR108 in pigs (Qin et al., 2016); and EGR2, PHYHIPL, SNORA70 and CIDEA in cattle (Abo-Ismail et al., 2018;Guo et al., 2014;Lengi & Corl, 2012;Taye et al., 2017). Using the xp-EHH approach, we found several genes previously documented in selection signatures in sheep populations, such as MGST1 located on sheep chromosome 3 (Rojas et al., 2016). ...
Article
Selection, both natural and artificial, leaves patterns on the genome during domestication of animals and leads to changes in allele frequencies among populations. Detecting genomic regions influenced by selection in livestock may assist in understanding the processes involved in genome evolution and discovering genomic regions related to traits of economic and ecological interests. In the current study, genetic diversity analyses were conducted on 34,206 quality‐filtered SNP positions from 450 individuals in 15 sheep breeds, including six indigenous breeds from the Middle East, namely Iranian Balouchi, Afshari, Moghani, Qezel, Karakas and Norduz, and nine breeds from Europe, namely East Friesian Sheep, Ile de France, Mourerous, Romane, Swiss Mirror, Spaelsau, Suffolk, Comisana and Engadine Red Sheep. The SNP genotype data generated by the Illumina OvineSNP50 Genotyping BeadChip array were used in this analysis. We applied two complementary statistical analyses, FST (fixation index) and xp‐EHH (cross‐population extended haplotype homozygosity), to detect selection signatures in Middle Eastern and European sheep populations. FST and xp‐EHH detected 629 and 256 genes indicating signatures of selection, respectively. Genomic regions identified using FST and xp‐EHH contained the CIDEA, HHATL, MGST1, FADS1, RTL1 and DGKG genes, which were reported earlier to influence a number of economic traits. Both FST and xp‐EHH approaches identified 60 shared genes as the signatures of selection, including four candidate genes (NT5E, ADA2, C8A and C8B) that were enriched for two significant Gene Ontology (GO) terms associated with the adenosine metabolic procedure. Knowledge about the candidate genomic regions under selective pressure in sheep breeds may facilitate identification of the underlying genes and enhance our understanding on these genes role in local adaptation.
... The logistic regression analyses further suggested that the homozygous sexually antagonistic alleles (HomSAE) have a direct influence on BTB infection risk in both males (positive influence) and females (negative influence). An influence of genetic background on BTB infection status in southern Kruger was also indicated in another microsatellite study [34] and we suspect that male-deleterious alleles were involved here as well. ...
Article
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In the African buffalo (Syncerus caffer) population of the Kruger National Park (South Africa) a primary sex-ratio distorter and a primary sex-ratio suppressor have been shown to occur on the Y chromosome. A subsequent autosomal microsatellite study indicated that two types of deleterious alleles with a negative effect on male body condition, but a positive effect on relative fitness when averaged across sexes and generations, occur genome-wide and at high frequencies in the same population. One type negatively affects body condition of both sexes, while the other acts antagonistically: it negatively affects male but positively affects female body condition. Here we show that high frequencies of male-deleterious alleles are attributable to Y-chromosomal distorter-suppressor pair activity and that these alleles are suppressed in individuals born after three dry pre-birth years, likely through epigenetic modification. Epigenetic suppression was indicated by statistical interactions between pre-birth rainfall, a proxy for parental body condition, and the phenotypic effect of homozygosity/heterozygosity status of microsatellites linked to male-deleterious alleles, while a role for the Y-chromosomal distorter-suppressor pair was indicated by between-sex genetic differences among pre-dispersal calves. We argue that suppression of male-deleterious alleles results in negative frequency-dependent selection of the Y distorter and suppressor; a prerequisite for a stable polymorphism of the Y distorter-suppressor pair. The Y distorter seems to be responsible for positive selection of male-deleterious alleles during resource-rich periods and the Y suppressor for positive selection of these alleles during resource-poor periods. Male-deleterious alleles were also associated with susceptibility to bovine tuberculosis, indicating that Kruger buffalo are sensitive to stressors such as diseases and droughts. We anticipate that future genetic studies on African buffalo will provide important new insights into gene fitness and epigenetic modification in the context of sex-ratio distortion and infectious disease dynamics.
... The significant negative health effects of BFDV and its recognition as a conservation threat globally has roused concern for parrots found in New Zealand and elsewhere [57][58][59][60][61]. Although human intervention in wildlife disease outbreaks (e.g., extirpation of vectors, immunization of hosts, and alteration of population distributions [62]) has been described, management agencies with limited resources may not have the funding required to respond, and recent evidence suggests that such intervention may have detrimental long-term effects [63,64]. Our study of red-crowned parakeets on Little Barrier Island illustrates the impact on an isolated, wild population of birds when a virulent viral pathogen is introduced and no management action is taken. ...
Article
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Pathogen outbreaks in the wild can contribute to a population's extinction risk. Concern over the effects of pathogen outbreaks in wildlife is amplified in small, threatened populations, where degradation of genetic diversity may hinder natural selection for enhanced immunocompetence. Beak and feather disease virus (BFDV) was detected for the first time in an island population of red-crowned parakeets (Cyanoramphus novaezelandiae) in 2008 on Little Barrier Island (Hauturu-o-Toi) of New Zealand. By 2013, the prevalence of the viral infection had significantly decreased within the population. We tested whether the population of red-crowned parakeets showed a selective response to BFDV, using neutral microsatellite and two immunity-associated genetic markers, the major histocompatibility complex (MHC) and Toll-like receptors (TLRs). We found evidence for selection at viral-associated TLR3; however, the ability of TLR3 to elicit an immune response in the presence of BFDV warrants confirmation. Alternatively, because red-crowned parakeet populations are prone to fluctuations in size, the decrease in BFDV prevalence over time may be attributed to the Little Barrier Island population dropping below the density threshold for viral maintenance. Our results highlight that natural processes such as adaptation for enhanced immunocompetence and/or density fluctuations are efficient mechanisms for reducing pathogen prevalence in a threatened, isolated population.
... Anthelminthic treatment was previously demonstrated to impact survival following bTB infection in a subset of this population [41]. Previous work has also demonstrated the two herds described here are not genetically distinct [37,60]. We therefore include the covariate 'herd' to account for large-scale environmental royalsocietypublishing.org/journal/rspb Proc. ...
Article
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Integrating biological processes across scales remains a central challenge in disease ecology. Genetic variation drives differences in host immune responses, which, along with environmental factors, generates temporal and spatial infection patterns in natural populations that epidemiologists seek to predict and control. However, genetics and immunology are typically studied in model systems, whereas population-level patterns of infection status and susceptibility are uniquely observable in nature. Despite obvious causal connections, organizational scales from genes to host outcomes to population patterns are rarely linked explicitly. Here we identify two loci near genes involved in macrophage (phagocyte) activation and pathogen degradation that additively increase risk of bovine tuberculosis infection by up to ninefold in wild African buffalo. Furthermore, we observe genotype-specific variation in IL-12 production indicative of variation in macrophage activation. Here, we provide measurable differences in infection resistance at multiple scales by characterizing the genetic and inflammatory variation driving patterns of infection in a wild mammal.
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Chapter
Cambridge Core - Ecology and Conservation - Conserving Africa's Mega-Diversity in the Anthropocene - edited by Joris P. G. M. Cromsigt
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Cambridge Core - Ecology and Conservation - Conserving Africa's Mega-Diversity in the Anthropocene - edited by Joris P. G. M. Cromsigt
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Cambridge Core - Ecology and Conservation - Conserving Africa's Mega-Diversity in the Anthropocene - edited by Joris P. G. M. Cromsigt
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Cambridge Core - Ecology and Conservation - Conserving Africa's Mega-Diversity in the Anthropocene - edited by Joris P. G. M. Cromsigt
Chapter
Cambridge Core - Ecology and Conservation - Conserving Africa's Mega-Diversity in the Anthropocene - edited by Joris P. G. M. Cromsigt
Chapter
Cambridge Core - Ecology and Conservation - Conserving Africa's Mega-Diversity in the Anthropocene - edited by Joris P. G. M. Cromsigt
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Introduced diseases can cause dramatic declines in-and even the loss of-natural populations. Extirpations may be followed by low recolonization rates, leading to inbreeding and a loss of genetic variation, with consequences on population viability. Conversely, extirpations may create vacant habitat patches that individuals from multiple source populations can colonize, potentially leading to an influx of variation. We tested these alternative hypotheses by sampling 15 colonies in a prairie dog metapopulation during 7 years that encompassed an outbreak of sylvatic plague, providing the opportunity to monitor genetic diversity before, during and after the outbreak. Analysis of nine microsatellite loci revealed that within the metapopulation, there was no change in diversity. However, within extirpated colonies, patterns varied: In half of the colonies, allelic richness after recovery was less than the preplague conditions, and in the other half, richness was greater than the preplague conditions. Finally, analysis of variation within individuals revealed that prairie dogs present in recolonized colonies had higher heterozygosity than those present before plague. We confirmed plague survivorship in six founders; these individuals had significantly higher heterozygosity than expected by chance. Collectively, our results suggest that high immigration rates can maintain genetic variation at a regional scale despite simultaneous extirpations in spatially proximate populations. Thus, virulent diseases may increase genetic diversity of host populations by creating vacant habitats that allow an influx of genetic diversity. Furthermore, even highly virulent diseases may not eliminate individuals randomly; rather, they may selectively remove the most inbred individuals.
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In an invasive species, selection for increased rates of dispersal at the expanding range front may favor the evolution of reduced investment into any trait that does not contribute to more rapid dispersal. Thus, populations at the invasion front may exhibit reduced investment into the immune system. To test this prediction, cane toads (Rhinella marina) from parents collected from populations across the toads’ invasion history in tropical Australia were raised in a standard environment. When their immune systems were challenged by injection of bacterial lipopolysaccharide, the toads’ metabolic rates rose by up to 40%. The magnitude of elevation in metabolic rate was lower in toads derived from the invasion front than in those from long-established populations. Our results support the hypothesis that an animal’s investment in immune defenses can be modified by selective forces that arise in the course of a biological invasion.
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Bovine tuberculosis due to Mycobacterium bovis is a zoonotic disease classically carried by cattle and spilling over into humans primarily by the ingestion of milk. However, in recent decades, there have been many endemic geographic localities where M. bovis has been detected infecting wildlife reservoirs, limiting the progress toward eradication of this disease from cattle. These include cervids in North America, badgers in Great Britain, feral pigs in Europe, brushtailed possums in New Zealand, and buffalo in South Africa. An overview of these wildlife hosts will provide insight into how these reservoirs maintain and spread the disease. In addition, the authors summarize the pathology, current ongoing methods for surveillance, and control. In many instances, it has proven to be more difficult to control or eradicate bovine tuberculosis in wild free-ranging species than in domesticated cattle. Furthermore, human influences have often contributed to the introduction and/or maintenance of the disease in wildlife species. Finally, some emerging themes regarding bovine tuberculosis establishment in wildlife hosts, as well as conclusions regarding management practices to assist in bovine tuberculosis control and eradication in wildlife, are offered.
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Possible evolutionary consequences of sport hunting have received relatively little con -sideration by wildlife managers. We reviewed the literature on genetic implications of sport hunting of terrestrial vertebrates and recommend research directions to address cur -rent uncertainties. Four potential effects can be ascribed to sport hunting: 1) it may alter the rate of gene flow among neighboring demes, 2) it may alter the rate of genetic drift through its effect on genetically effective population size, 3) it may decrease fitness by deliberately culling individuals with traits deemed undesirable by hunters or managers, and 4) it may inadvertently decrease fitness by selectively removing individuals with traits desired by hunters. Which, if any, of these effects are serious concerns depends on the nature and intensity of harvest as well as the demographic characteristics and breeding system of the species at issue. Undesirable genetic consequences from hunting have been documented in only a few cases, and we see no urgency. However, studies specif -ically investigating these issues have been rare, and such consequences require careful analysis and long time periods to detect. Existing information is sufficient to suggest that hunting regimes producing sex-and age-specific mortality patterns similar to those occur -ring naturally, or which maintain demographic structures conducive to natural breeding patterns, will have fewer long-term evolutionary consequences than those producing highly uncharacteristic mortality patterns.
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Understanding which parts of the genome have been most influenced by adaptive evolution remains an unsolved puzzle. Some evidence suggests that selection has the greatest impact on regions of the genome that interact with other evolving genomes, including loci that are involved in host-parasite co-evolutionary processes. In this study, we used a population genetic approach to test this hypothesis by comparing DNA sequences of 30 putative immune system genes in the crustacean Daphnia pulex with 24 non-immune system genes. In support of the hypothesis, results from a multilocus extension of the McDonald-Kreitman (MK) test indicate that immune system genes as a class have experienced more adaptive evolution than non-immune system genes. However, not all immune system genes show evidence of adaptive evolution. Additionally, we apply single locus MK tests and calculate population genetic parameters at all loci in order to characterize the mode of selection (directional versus balancing) in the genes that show the greatest deviation from neutral evolution. Our data are consistent with the hypothesis that immune system genes undergo more adaptive evolution than non-immune system genes, possibly as a result of host-parasite arms races. The results of these analyses highlight several candidate loci undergoing adaptive evolution that could be targeted in future studies.
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Pathogens that are transmitted between wildlife, livestock and humans present major challenges for the protection of human and animal health, the economic sustainability of agriculture, and the conservation of wildlife. Mycobacterium bovis, the aetiological agent of bovine tuberculosis (TB), is one such pathogen. The incidence of TB in cattle has increased substantially in parts of Great Britain in the past two decades, adversely affecting the livelihoods of cattle farmers and potentially increasing the risks of human exposure. The control of bovine TB in Great Britain is complicated by the involvement of wildlife, particularly badgers (Meles meles), which appear to sustain endemic infection and can transmit TB to cattle. Between 1975 and 1997 over 20,000 badgers were culled as part of British TB control policy, generating conflict between conservation and farming interest groups. Here we present results from a large-scale field trial that indicate that localized badger culling not only fails to control but also seems to increase TB incidence in cattle.
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The evolution of host resistance to parasites, shaped by associated fitness costs, is crucial for epidemiology and maintenance of genetic diversity. Selection imposed by multiple parasites could be a particularly strong constraint, as hosts either accumulate costs of multiple specific resistances or evolve a more costly general resistance mechanism. We used experimental evolution to test how parasite heterogeneity influences the evolution of host resistance. We show that bacterial host populations evolved specific resistance to local bacteriophage parasites, regardless of whether they were in single or multiple-phage environments, and that hosts evolving with multiple phages were no more resistant to novel phages than those evolving with single phages. However, hosts from multiple-phage environments paid a higher cost, in terms of population growth in the absence of phage, for their evolved specific resistances than those from single-phage environments. Given that in nature host populations face selection pressures from multiple parasite strains and species, our results suggest that costs may be even more critical in shaping the evolution of resistance than previously thought. Furthermore, our results highlight that a better understanding of resistance costs under combined control strategies could lead to a more 'evolution-resistant' treatment of disease.
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Infectious diseases are increasingly recognised to be a major threat to biodiversity. Disease management tools such as control of animal movements and vaccination can be used to mitigate the impact and spread of diseases in targeted species. They can reduce the risk of epidemics and in turn the risks of population decline and extinction. However, all species are embedded in communities and interactions between species can be complex, hence increasing the chance of survival of one species can have repercussions on the whole community structure. In this study, we use an example from the Serengeti ecosystem in Tanzania to explore how a vaccination campaign against Canine Distemper Virus (CDV) targeted at conserving the African lion (Panthera leo), could affect the viability of a coexisting threatened species, the cheetah (Acinonyx jubatus). Assuming that CDV plays a role in lion regulation, our results suggest that a vaccination programme, if successful, risks destabilising the simple two-species system considered, as simulations show that vaccination interventions could almost double the probability of extinction of an isolated cheetah population over the next 60 years. This work uses a simple example to illustrate how predictive modelling can be a useful tool in examining the consequence of vaccination interventions on non-target species. It also highlights the importance of carefully considering linkages between human-intervention, species viability and community structure when planning species-based conservation actions.
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Detecting artificial selection in the genome of domesticated species can not only shed light on human history but can also be beneficial to future breeding strategies. Evidence for selection has been documented in domesticated species including maize and rice, but few studies have to date detected signals of artificial selection in the Sorghum bicolor genome. Based on evidence that domesticated S. bicolor and its wild relatives show significant differences in endosperm structure and quality, we sequenced three candidate seed storage protein (kafirin) loci and three candidate starch biosynthesis loci to test whether these genes show non-neutral evolution resulting from the domestication process. We found strong evidence of non-neutral selection at the starch synthase IIa gene, while both starch branching enzyme I and the beta kafirin gene showed weaker evidence of non-neutral selection. We argue that the power to detect consistent signals of non-neutral selection in our dataset is confounded by the absence of low frequency variants at four of the six candidate genes. A future challenge in the detection of positive selection associated with domestication in sorghum is to develop models that can accommodate for skewed frequency spectrums.
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Most hosts are infected with multiple parasites, and responses of the immune system to co-occurring parasites may influence disease spread. Helminth infection can bias the host immune response toward a T-helper type 2 (Th2) over a type 1 (Th1) response, impairing the host’s ability to control concurrent intracellular microparasite infections and potentially modifying disease dynamics. In humans, immune-mediated interactions between helminths and microparasites can alter host susceptibility to diseases such as HIV, tuberculosis (TB), and malaria. However, the extent to which similar processes operate in natural animal populations and influence disease spread remains unknown. We used cross-sectional, experimental, and genetic studies to show that gastrointestinal nematode infection alters immunity to intracellular microparasites in free-ranging African buffalo (Syncerus caffer). Buffalo that were more resistant to nematode infection had weaker Th1 responses, there was significant genotypic variation in nematode resistance, and anthelminthic treatment enhanced Th1 immunity. Using a disease dynamic model parameterized with empirical data, we found that nematode-induced immune suppression can facilitate the invasion of bovine TB in buffalo. In the absence of nematodes, TB failed to invade the system, illustrating the critical role nematodes may play in disease establishment. Our results suggest that helminths, by influencing the likelihood of microparasite invasion, may influence patterns of disease emergence in the wild.
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Interleukin-4 (IL4) is a secreted immunoregulatory cytokine critically involved in host protection from parasitic helminths 1. Reasoning that helminths may have evolved mechanisms to antagonize IL4 to maximize their dispersal, we explored mammalian IL4 evolution. This analysis revealed evidence of diversifying selection at 15 residues, clustered in epitopes responsible for IL4 binding to its Type I and Type II receptors. Such a striking signature of selective pressure suggested either recurrent episodes of pathogen antagonism or ligand/receptor co-evolution. To test the latter possibility, we performed detailed functional analysis of IL4 allotypes expressed by Mus musculus musculus and Mus musculus castaneus, which happen to differ at 5 residues (including three at positively selected sites) in and adjacent to the site 1 epitope that binds the IL4Ralpha subunit shared by the Type I and Type II IL4 receptors. We show that this intra-species variation affects the ability of IL4 neither to bind IL4 receptor alpha (IL4Ralpha) nor to signal biological responses through its Type I receptor. Our results - reminiscent of clustered positively selected sites revealing functionally important residues at host-virus interaction interfaces - are consistent with IL4 having evolved to avoid recurrent pathogen antagonism, while maintaining the capacity to bind and signal through its cognate receptor. This work exposes what may be a general feature of evolutionary conflicts fought by pathogen antagonists at host protein-protein interaction interfaces involved in immune signaling: the emergence of receptor-binding ligand epitopes capable of buffering amino acid variation.
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The basis for understanding the characteristics of gene functional categories in chicken has been enhanced by the ongoing sequencing of the zebra finch genome, the second bird species to be extensively sequenced. This sequence provides an avian context for examining how variation in chicken has evolved since its divergence from its common ancestor with zebra finch as well as well as a calibrating point for studying intraspecific diversity within chicken. Immune genes have been subject to many selective processes during their evolutionary history: this gene class was investigated here in a set of orthologous chicken and zebra finch genes with functions assigned from the human ortholog. Tests demonstrated that nonsynonymous sites at immune genes were highly conserved both in chicken and on the avian lineage. McDonald-Kreitman tests provided evidence of adaptive evolution and a higher rate of selection on fixation of nonsynonymous substitutions at immune genes compared to that at non-immune genes. Further analyses showed that GC content was much higher in chicken than in zebra finch genes, and was significantly elevated in both species' immune genes. Pathogen challenges are likely to have driven the selective forces that have shaped variation at chicken immune genes, and continue to restrict diversity in this functional class.
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There is growing concern about the evolutionary consequences of human harvesting on phenotypic trait quality in wild populations. Undesirable consequences are especially likely with trophy hunting because of its strong bias for specific phenotypic trait values, such as large antlers in cervids and horns in bovids. Selective hunting can cause a decline in a trophy trait over time if it is heritable, thereby reducing the long-term sustainability of the activity itself. How can we build a sustainable trophy hunting tradition without the negative trait-altering effects? We used an individual-based model to explore whether selective compensatory culling of ‘low quality’ individuals at an early life stage can facilitate sustainability, as suggested by information from managed game populations in eastern and central Europe. Our model was rooted in empirical data on red deer, where heritability of sexual ornaments has been confirmed and phenotypic quality can be assessed by antler size in individuals as young as 1 year. Simulations showed that targeted culling of low-quality yearlings could counter the selective effects of trophy hunting on the distribution of the affected trait (e.g. antler or horn size) in prime-aged individuals. Assumptions of trait heritability and young-to-adult correlation were essential for compensation, but the model proved robust to various other assumptions and changes to input parameters. The simulation approach allowed us to verify responses as evolutionary changes in trait values rather than short-term consequences of altered age structure, density and viability selection. We conclude that evolutionarily enlightened management may accommodate trophy hunting. This has far reaching implications as income from trophy hunting is often channelled into local conservation efforts and rural economies. As an essential follow-up, we recommend an analysis of the effects of trophy hunting in conjunction with compensatory culling on the phenotypic and underlying genetic variance of the trophy trait.
Chapter
This book contains 16 chapters. Topics covered are: patents, trade secrets and other forms of intellectual property rights; advent of animal patents: innovation and controversy in the engineering and ownership of life; economics of patents; access to data and intellectual property; global intellectual property: international developments in animal patents; public university, intellectual property and agricultural R and D; lessons from the patenting of plants; patenting and sequencing the genome; open source and other software intellectual property models; animals, ethics and patents; development of a genetic marker for litter size in the pig: a case study; development and commercialization of a genetic marker for marbling of beef in cattle: a case study; research and patent perspective of nuclear transfer cloning: case studies; dairy cattle test day models: a case study; development and commercialization of software for genetic improvement programmes: a case study; final thoughts.
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Emerging infectious diseases have become an important challenge for wildlife ecologists and managers. Management actions to control these diseases are usually directed at the parasite, the host population, or a key component of the environment, with the goal of reducing disease exposure and transmission. Control methods directed at the host population, however, remain limited in approach (e.g. vaccination, population reduction, test-and-remove) and scope, by financial, logistical, ethical and political constraints. Furthermore, these control methods have often been implemented without due consideration of how host ecology and behaviour may influence disease dynamics. This chapter highlights how host population structure and social organisation affect parasite transmission and prevalence. Traditionally, variation in disease prevalence among species, genders, and ages may have been explained by immunological differences in susceptibility. However, ecological and behavioural factors can also affect the rates and routes of parasite transmission and potential control options. Using this information, future control efforts may be improved by focusing on subsets of individuals, areas, environmental factors, or times of year that are most important in the propagation and persistence of a pathogen.
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Parasites and pathogens of wildlife can threaten biodiversity, infect humans and domestic animals, and cause significant economic losses, providing incentives to manage wildlife diseases. Recent insights from disease ecology have helped transform our understanding of infectious disease dynamics and yielded new strategies to better manage wildlife diseases. Simultaneously, wildlife disease management (WDM) presents opportunities for large-scale empirical tests of disease ecology theory in diverse natural systems. To assess whether the potential complementarity between WDM and disease ecology theory has been realized, we evaluate the extent to which specific concepts in disease ecology theory have been explicitly applied in peer-reviewed WDM literature. While only half of WDM articles published in the past decade incorporated disease ecology theory, theory has been incorporated with increasing frequency over the past 40 years. Contrary to expectations, articles authored by academics were no more likely to apply disease ecology theory, but articles that explain unsuccessful management often do so in terms of theory. Some theoretical concepts such as density-dependent transmission have been commonly applied, whereas emerging concepts such as pathogen evolutionary responses to management, biodiversity–disease relationships and within-host parasite interactions have not yet been fully integrated as management considerations. Synthesis and applications. Theory-based disease management can meet the needs of both academics and managers by testing disease ecology theory and improving disease interventions. Theoretical concepts that have received limited attention to date in wildlife disease management could provide a basis for improving management and advancing disease ecology in the future.
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Abstract This study examines the population biology of African buffalo (Syncerus caffer Sparrman) at Hluhluwe-iMfolozi Park (HiP), South Africa. An analysis of buffalo census data covering the period from 1956 to 2006 shows that the population has a moderate intrinsic growth rate at around 12% per annum, which is similar to growth rates of buffalo populations measured elsewhere. The population is subject to density dependence when the number of buffalo in the park exceeds approximately 3500 animals. In most years over the past 25 years, the population has exceeded this threshold, and net annual population growth has averaged around 5%. Periods of buffalo population decline always coincided with heavy buffalo removals, suggesting limited resilience of the population to such disturbances. Demographic data from 826 buffalo in 12 herds, captured in 2001–2002, were used to parameterize an age-structured buffalo population model. The model yields an annual population growth rate of 4.05%, similar to recent growth estimates from buffalo censuses at HiP. The predicted stable age distribution is very similar to the age distribution observed in the captured population sample. Elasticity analysis of the model indicates that population growth in buffalo is most sensitive to adult and juvenile survival, and less sensitive to recruitment parameters and survival of old animals. Buffalo populations might therefore be expected to be more vulnerable to mortality factors affecting prime-aged adults than those affecting juveniles or senescent individuals.
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Infectious diseases can bring, about population declines and local host extinctions, contributing significantly to the global biodiversity crisis. Nonetheless, studies measuring population-level effects of pathogens in wild host populations are rare, and taxonomically biased toward avian hosts and macroparasitic infections. We investigated the effects of bovine tuberculosis (bTB), caused by the bacterial pathogen. Mycobacterium bovis, on African buffalo (Syncerus caffer) at Hluhluwe-iMfolozi Park, South Africa. We tested 1180 buffalo for bTB infection between May 2000 and November 2001. Most infections were mild, confirming the chronic nature of the disease in buffalo. However, our data indicate that bTB affects both adult survival and fecundity. Using an age-structured population model, we demonstrate that the pathogen can reduce population growth rate drastically; yet its effects appear difficult to detect at the population level: bTB causes no conspicuous mass mortalities or fast population declines
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In this study, the ecological effects of culling programs are considered in the context of rodent pest management. Despite the escalation of rodent problems globally, over the past quarter of a century there have not been many new developments in culling programs directed at managing these populations. There is a strong reliance on broad scale use of chemical rodenticides or other lethal methods of control. The ecological consequences of culling programs based on chemical rodenticides and bounty systems are considered. Although rodents cause tremendous economic hardship to people on a continental scale, usually less than 10% of species cause substantial impacts. Indeed, many species of rodent provide important “ecological services” and, given that culling programs rarely distinguish between rodent species, often the non-pest rodents are at grave risk. Rodent control is conducted with little appreciation of what proportion of the population would need to be culled for a significant reduction in economic damage. In Indonesian rice fields, once rodent densities are high then a reduction in yield loss from 30% to 15% would require more than 75% of the population to be culled; a reduction to less than 5% yield loss would require more than a 95% cull. The negative ecological consequences of culling can be better managed if the method is specifically tailored to the species that need to be managed. A greater emphasis on ecologically-based rodent management would assist markedly in reducing the unwanted and unintended effects of culling.
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1. Harvesting of large mammals is usually not random, and directional selection has been identified as the main cause of rapid evolution. However, selective harvesting in meat and recreational hunting cultures does not automatically imply directional selection for trait size. 2. Harvesting selectivity is more than a matter of hunter preference. Selection is influenced by management regulations, hunting methods, animal trait variance, behaviour and abundance. Most studies of hunter selection only report age- or sex-specific selection, or differences in trait size selection among hunting methods or groups of hunters, rather than trait size relative to the age-specific means required for directional selection. 3. Synthesis and applications. Managers aiming to avoid rapid evolution should not only consider directional selection and trophy hunting but also mitigate other important evolutionary forces such as harvesting intensity per se, and sexual selection processes that are affected by skewed sex ratios and age structures.
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Recent increases in the magnitude and rate of environmental change, including habitat loss, climate change and overexploitation, have been directly linked to the global loss of biodiversity. Wildlife extinction rates are estimated to be 100–1000 times greater than the historical norm, and up to 50% of higher taxonomic groups are critically endangered. While many types of environmental changes threaten the survival of species all over the planet, infectious disease has rarely been cited as the primary cause of global species extinctions. There is substantial evidence, however, that diseases can greatly impact local species populations by causing temporary or permanent declines in abundance. More importantly, pathogens can interact with other driving factors, such as habitat loss, climate change, overexploitation, invasive species and environmental pollution to contribute to local and global extinctions. Regrettably, our current lack of knowledge about the diversity and abundance of pathogens in natural systems has made it difficult to establish the relative importance of disease as a significant driver of species extinction, and the context when this is most likely to occur. Here, we review the role of infectious diseases in biological conservation. We summarize existing knowledge of disease-induced extinction at global and local scales and review the ecological and evolutionary forces that may facilitate disease-mediated extinction risk. We suggest that while disease alone may currently threaten few species, pathogens may be a significant threat to already-endangered species, especially when disease interacts with other drivers. We identify control strategies that may help reduce the negative effects of disease on wildlife and discuss the most critical challenges and future directions for the study of infectious diseases in the conservation sciences.
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DNA degradation, low DNA concentrations and primer-site mutations may result in the incorrect assignment of microsatellite genotypes, potentially biasing population genetic analyses. MICRO-CHECKER is WINDOWS(R)-based software that tests the genotyping of microsatellites from diploid populations. The program aids identification of genotyping errors due to nonamplified alleles (null alleles), short allele dominance (large allele dropout) and the scoring of stutter peaks, and also detects typographic errors. MICRO-CHECKER estimates the frequency of null alleles and, importantly, can adjust the allele and genotype frequencies of the amplified alleles, permitting their use in further population genetic analysis.
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Yellowstone bison (Bison bison bison) are managed to reduce the risk of brucellosis (Brucella abortus) transmission to cattle while allowing some migration out of Yellowstone National Park to winter ranges in Montana. Intensive management near conservation area boundaries maintained separation between bison and cattle, with no transmission of brucellosis. However, brucellosis prevalence in the bison population was not reduced and the management plan underestimated bison abundance, distribution, and migration, which contributed to larger risk management culls (total >3000 bison) than anticipated. Culls differentially affected breeding herds and altered gender structure, created reduced female cohorts, and dampened productivity. The ecological future of plains bison could be significantly enhanced by resolving issues of disease and social tolerance for Yellowstone bison so that their unique wild state and adaptive capabilities can be used to synergize the restoration of the species. We recommend several adaptive management adjustments that could be implemented to enhance the conservation of plains bison and reduce brucellosis infection. These findings and recommendations are pertinent to wood bison (Bison bison athabascae), European bison (Bison bonasus), and other large ungulates worldwide that are managed using best practices within a risk framework.
Article
1. The incidence of bovine tuberculosis (TB) in British cattle has risen markedly over the last two decades. Failure to control the disease in cattle has been linked to the persistence of a reservoir of infection in European badgers Meles meles, a nationally protected species. Although badger culling has formed a component of British TB control policy for many years, a recent large-scale randomized field experiment found that TB incidence in cattle was no lower in areas subject to localized badger culling than in nearby areas where no experimental culls occurred. Indeed, analyses indicated that cattle incidence was higher in culled areas. 2. One hypothesis advanced to explain this pattern is that localized culling disrupted badgers' territorial behaviour, potentially increasing the rate of contact between cattle and infected badgers. This study evaluated this hypothesis by investigating badger activity and spatial organization in 13 study areas subjected to different levels of culling. Badger home ranges were mapped by feeding colour-marked baits at badger dens and measuring the geographical area in which colour-marked faeces were retrieved. 3. Badger home ranges were consistently larger in culling areas. Moreover, in areas not subjected to culling, home range sizes increased with proximity to the culling area boundary. Patterns of overlap between home ranges were also influenced by culling. 4. Synthesis and applications. This study demonstrates that culling badgers profoundly alters their spatial organization as well as their population density. These changes have the potential to influence contact rates between cattle and badgers, both where culls occur and on adjoining land. These results may help to explain why localized badger culling appears to have failed to control cattle TB, and should be taken into account in determining what role, if any, badger culling should play in future control strategies.
Article
Infectious disease is an emerging threat that conservationists are ill-equipped to manage. The threat is greatest for small populations, which can be driven to extinction by virulent pathogens; these are usually generalist pathogens that ‘spill over’ from other host species, often domestic animals. Recent attempts at disease control have taken a variety of forms, some directed at threatened hosts themselves, and others involving reservoir hosts. Thus far, few such attempts have demonstrated clear benefits of intervention, often because they were ‘crisis management’ tactics allowing no comparison with untreated controls. Design of future strategies is hampered by a lack of basic information concerning the pathogens that represent serious threats, their epidemiology in multiple-host systems, and the vaccination or treatment protocols likely to be most effective under field conditions. In general, vaccination and treatment will be most valuable in tiny populations facing very high extinction risks. However, interventions that are poorly planned or under-funded have the potential to do more harm than good. In larger populations, or over larger areas, intensive management may be inappropriate, unsustainable, or simply impractical. In these circumstances, managing population size, structure or contact between host species could offer promising alternatives to intervention.
Article
The joint effects of linkage and epistasis (interaction between non-allelic genes in determining fitness) have been examined for two-locus polymorphisms. The general results are of the following nature: (1) Gene frequencies change toward a stable equilibrium condition which corresponds to a local maximum in mean adaptive value. This change occurs in such a way that the rate of increase of mean adaptive value is not maximum. That is, the trajectory of gene frequency changes is not the "steepest path" on the adaptive surface. (2) In the absence of epistasis, linkage does not affect the final equilibrium of the population. (3) When epistasis is present, linkage must be fairly tight in order for there to be any effect on the final equilibrium. The amount of recombination allowed for such cases is, in general, a function of epistatic deviations. (4) If linkage is tighter than the value demanded by the magnitude of epistatic deviations, there may be permanent linkage disequilibrium of considerable magnitude, and the gene frequencies may also be affected. (5) There are some cases where a stable equilibrium is possible only with a tight linkage. Without such linkage complication, there will be no intermediate gene frequency stable equilibrium. (6) The approach to the equilibrium condition is affected by linkage irrespective of whether there is epistasis although the effect is greater when epistasis is present.
Book
Spectacular progress has been made recently in the study of evolution at the molecular level, primarily due to new biochemical techniques such as gene cloning and DNA sequencing. In this book, the author summarizes new developments and seeks to unify studies of evolutionary histories of organisms and the mechanisms of evolution into a single science - molecular evolutionary genetics.
Article
Bovine tuberculosis (BTB) is a considerable health threat to livestock keepers and general communities in many developing countries. Information on genetic resistance or susceptibility because of polymorphisms of candidate genes could be used in making selection decisions for breeding disease tolerant/resistant animals. Here, we investigated associations between polymorphisms at the solute carrier family 11 (proton-coupled divalent metal ion transporters), member 1 gene (SLC11A1, previously known as natural resistant associated macrophage protein 1, NRAMP1), with BTB phenotypes in Chadian cattle. Phenotypes were (i) single intradermal comparative cervical tuberculin test (SICCT) outcome, (ii) presence of gross visible lung lesions, (iii) a bacteriological culture test outcome and (iv) a predicted true BTB infection status using a Bayesian model. All traits were recorded as binary (presence or absence) traits. A total of 211 cattle were genotyped for a microsatellite within the SLC11A1 candidate gene. Standard linear and threshold-liability models regressing BTB traits on copy number of SLC11A1 alleles revealed statistically significant effects of SLC11A1 alleles (P < 0.001) on most BTB traits. Polymorphisms (alleles 211, 215 and 217) are significantly related to lower incidence of BTB traits in Chadian cattle. This is the first study to report the association of SLC11A1 gene polymorphisms with BTB traits in Chadian or any other African cattle breeds.
Article
Previous studies of immunity in wild populations have focused primarily on genes of the major histocompatibility complex (MHC); however, studies of model species have identified additional immune-related genes that also affect fitness. In this study, we sequenced five non-MHC immune genes in six greater prairie-chicken (Tympanuchus cupido) populations that have experienced varying degrees of genetic drift as a consequence of population bottlenecks and fragmentation. We compared patterns of geographic variation at the immune genes with six neutral microsatellite markers to investigate the relative effects of selection and genetic drift. Global F(ST) outlier tests identified positive selection on just one of five immune genes (IAP-1) in one population. In contrast, at other immune genes, standardized G'(ST) values were lower than those at microsatellites for a majority of pairwise population comparisons, consistent with balancing selection or with species-wide positive or purifying selection resulting in similar haplotype frequencies across populations. The effects of genetic drift were also evident as summary statistics (e.g., Tajima's D) did not differ from neutrality for the majority of cases, and immune gene diversity (number of haplotypes per gene) was correlated positively with population size. In summary, we found that both genetic drift and selection shaped variation at the five immune genes, and the strength and type of selection varied among genes. Our results caution that neutral forces, such as drift, can make it difficult to detect current selection on genes.
Article
There are numerous examples demonstrating that selection has greatly influenced phenotypes in wild-harvested species. Here, a significant reduction in horn size in trophy desert bighorn sheep rams over 30 years in a reintroduced population in Aravaipa Canyon, Arizona is documented. After examining the potential effects of a detrimental change in the environment, inbreeding depression, and hunter-caused evolutionary change, it appears that environmental deterioration, apparently from the effects of drought, may be a major cause of the decline in horn size. In particular, the reduction in ram horn size is positively associated with reduced winter lifetime rainfall over the 3 decades. Over the same period, the demographic indicator lamb-to-ewe ratio has also declined in the Aravaipa population. On the other hand, lamb-to-ewe ratio has not declined statewide in Arizona, and the population size in Aravaipa appears to be increasing, suggesting local- and trait-specific effects. Using a theoretical context, neither inbreeding depression nor hunter selection by themselves appear to the sole causes of the lower horn size. However, some combination of environmental factors, inbreeding depression, and hunter selection may have caused the decrease in observed horn size. It is not clear what management actions might be successful in countering the environmental effects on horn size, but supplemental feeding and cattle removal are suggested while translocation is suggested to counter the effects of inbreeding depression and reduced hunting and translocation are suggested to counter the effects of hunter selection.
Article
Patterns of selection acting on immune defence genes have recently been the focus of considerable interest. Yet, when it comes to vertebrates, studies have mainly focused on the acquired branch of the immune system. Consequently, the direction and strength of selection acting on genes of the vertebrate innate immune defence remain poorly understood. Here, we present a molecular analysis of selection on an important receptor of the innate immune system of vertebrates, the Toll-like receptor 2 (TLR2), across 17 rodent species. Although purifying selection was the prevalent evolutionary force acting on most parts of the rodent TLR2, we found that codons in close proximity to pathogen-binding and TLR2-TLR1 heterodimerization sites have been subject to positive selection. This indicates that parasite-mediated selection is not restricted to acquired immune system genes like the major histocompatibility complex, but also affects innate defence genes. To obtain a comprehensive understanding of evolutionary processes in host-parasite systems, both innate and acquired immunity thus need to be considered.
Article
To measure the economic costs and benefits of scaling up tuberculosis (TB) control under the Revised National Tuberculosis Control Programme (RNTCP) in India. Modelling based on country-level programme and epidemiological data from 1997 to 2006. The scale-up of TB control in India has resulted in a total health benefit of 29.2 million disability-adjusted life years (DALYs), including 1.3 million deaths averted. In 2006, the burden of TB measured in terms of DALYs lost would have been 1.8 times higher in the absence of the programme. The total gain in economic well-being from TB control is estimated at US$88.1 billion over the 1997-2006 10-year period. Total public expenditure on TB control over this period amounted to US$768 million, with the RNTCP accounting for US$299 million and other health sector costs accounting for US$469 million. The cost of TB control averaged just US$26 per DALY gained over 1997-2006 and generated a return of US$115 per dollar spent. The scale-up of TB control has been a very cost-effective strategy for improving the health status of India's population, while the return on investment has been exceptional from a societal perspective.
Article
Using Atlantic salmon (Salmo salar) as a model system, we investigated whether 18 microsatellites tightly linked to immune-relevant genes have experienced different selection pressures than 76 loci with no obvious association with immune function. Immune-relevant loci were identified as outliers by two outlier tests significantly more often than nonimmune linked loci (22% vs. 1.6%). In addition, the allele frequencies of immune relevant markers were more often correlated with latitude and temperature. Combined, these results support the hypothesis that immune-relevant loci more frequently exhibit footprints of selection than other loci. They also indicate that the correlation between immune-relevant loci and latitude may be due to temperature-induced differences in pathogen-driven selection or some other environmental factor correlated with latitude.
Article
Major histocompatibility complex (MHC) genes have been put forward as a model for studying how genetic diversity is maintained in wild populations. Pathogen-mediated selection (PMS) is believed to generate the extraordinary levels of MHC diversity observed. However, establishing the relative importance of the three proposed mechanisms of PMS (heterozygote advantage, rare-allele advantage and fluctuating selection) has proved extremely difficult. Studies have attempted to differentiate between mechanisms of PMS using two approaches: (i) comparing MHC diversity with that expected under neutrality and (ii) relating MHC diversity to pathogen regime. Here, we show that in many cases the same predictions arise from the different mechanisms under these approaches, and that most studies that have inferred one mechanism of selection have not fully considered the alternative explanations. We argue that, while it may be possible to demonstrate that particular mechanisms of PMS are occurring, resolving their relative importance within a system is probably impossible. A more realistic target is to continue to demonstrate when and where the different mechanisms of PMS occur, with the aim of determining their relative importance across systems. We put forward what we believe to be the most promising approaches that will allow us to progress towards achieving this.