Subspecific relationships and genetic structure in the spotted owl

Hierarchical genetic structure was examined in the three geographically-defined subspecies of spotted owl (Strix occidentalis) to define relationships among subspecies and quantify variation within and among regional and local populations. Sequences (522 bp) from domains I and II of the mitochondrial control region were analyzed for 213 individuals from 30 local breeding areas. Results confirmed significant differences between northern spotted owls and the other traditional geographically defined subspecies but did not provide support for subspecific level differences between California and Mexican spotted owls. Divergence times among subspecies estimated with a 936 bp portion of the cytochrome b gene dated Northern and California/Mexican spotted owl divergence time to 115,000–125,000 years ago, whereas California/Mexican spotted owl divergence was estimated at 15,000 years ago. Nested clade analyses indicated an association between California spotted owl and Mexican spotted owl haplotypes, implying historical contact between the two groups. Results also identified a number of individuals geographically classified as northern spotted owls (S. o. caurina) that contained haplotypes identified as California spotted owls (S. o. caurina). Among all northern spotted owls sampled (n=131), 12.9% contained California spotted owl haplotypes. In the Klamath region, which is the contact zone between the two subspecies, 20.3% (n=59) of owls were classified as California spotted owls. The Klamath region is a zone of hybridization and speciation for many other taxa as well. Analyses of population structure indicated gene flow among regions within geographically defined subspecies although there was significant differentiation among northern and southern regions of Mexican spotted owls. Among all areas examined, genetic diversity was not significantly reduced except in California spotted owls where the southern region consists of one haplotype. Our results indicate a stable contact zone between northern and California spotted owls, maintaining distinct subspecific haplotypes within their traditional ranges. This supports recovery efforts based on the traditional subspecies designation for the northern spotted owl. Further, although little variation was found between California and Mexican spotted owls, we suggest they should be managed separately because of current isolation between groups.     

PHYLOGEOGRAPHY OF SPOTTED OWL (STRIX OCCIDENTALIS) POPULATIONS BASED ON MITOCHONDRIAL DNA SEQUENCES: GENE FLOW,GENETIC STRUCTURE,AND A NOVEL BIOGEOGRAPHIC PATTERN

Mitochondrial DNA control region sequences of spotted owls (Strix occidentalis) allowed us to investigate gene flow, genetic structure, and biogeographic relationships among these forest-dwelling birds of western North America Estimates of gene flow based on genetic partitioning and the phylogeography of haplotypes indicate substantial dispersal within three long-recognized subspecies. However, patterns of individual phyletic relationships indicate a historical absence of gene flow among the subspecies, which are essentially monophyletic. The pattern of haplotype coalescence enabled us to identify the approximate timing and direction of a recent episode of gene flow from the Sierra Nevada to the northern coastal ranges. The three subspecies comprise phylogenetic species, and the northern spotted owl (S. o. caurina) is sister to a clade of California (S. o. occidentalis) plus Mexican spotted owls (S o lucida); this represents a novel biogeographic pattern within birds. The California spotted owl had substantially lower nucleotide diversity than the other two subspecies; this result is inconsistent with present patterns of population density A causal explanation requires postulating a severe bottleneck or a selective sweep, either of which was confined to only one geographic region.     

Review of the effects of barred owls on spotted owls

Barred owls (Strix varia) are forest-dwelling owls, native to eastern North America, with populations that expanded westward into the range of the spotted owl (Strix occidentalis). Barred owls exert an overwhelmingly negative influence on spotted owls, thereby threatening spotted owl population viability where the species co-occur. In this review, we provide an overview of the barred owl's range expansion and detail and synthesize previously published literature on spotted and barred owls within the range of the spotted owl as related to potential future outcomes for the northern spotted owl (S. o. caurina). We include research on diet, habitat use and selection, effects of barred owls on spotted owl demography and behavior, hybridization with spotted owls, parasites, contemporary management, and future research needs for spotted owl populations given continued barred owl expansion throughout western North America. Our literature review and synthesis should provide managers with the information necessary to develop strategies that mitigate deleterious effects of barred owls at local and landscape scales. © 2019 The Wildlife Society.     

The Invasion of Barred Owls and its Potential Effect on the Spotted Owl: a Conservation Conundrum

The spotted owl (Strix occidentalis) is a threatened species in many areas of its western North American range. Concomitant with its decline has been a rapid invasion of its range and habitat by barred owls (Strix varia), a native species that was restricted, until relatively recently, to eastern North America. We assess the theoretical potential for negative interactions between these two owls by examining size dimorphism and ecological relationships within various owl assemblages throughout the world. We then review the anecdotal, natural history, modeling, and experimental evidence that suggest barred owls may negatively affect spotted owls with at least a potential for the competitive exclusion of spotted owls by barred owls throughout all or part of the former’2019;s range. While it is widely accepted that barred owls are either causing or exacerbating declines of spotted owl populations, there are confounding factors, such as habitat loss and bad weather that also may contribute to declines of spotted owls. Both theory and empirical information suggest that barred owls are likely to have negative effects on spotted owl range and density, but the degree of the impact is not predictable. There is a conservation conundrum here, in that the barred owl is a native species that has expanded its range westwards, either naturally or with a degree of human facilitation, and now constitutes a major threat to the viability of another native species, the threatened spotted owl. We propose that only through carefully designed experiments involving removal of barred owls will we be able to determine if recent declines in spotted owl populations are caused by barred owls or by other factors. It is rare in conservation science that replicate study areas exist for which we also have long-standing demographic information, as is the case with the spotted owl. Removal experiments would take advantage of the wealth of data on spotted owls, and allow ecologists to assess formally the impacts of an invasive species on a threatened species, as well as to suggest mitigation measures.     

Habitat selection by northern spotted owls in mixed-coniferous forests

Conservation planning for the federally threatened northern spotted owl (Strix occidentalis caurina) requires an ability to predict their responses to existing and future habitat conditions. To inform such planning we modeled habitat selection by northern spotted owls based upon fine-scale (approx. 1.0 ha) characteristics within stands comprised primarily of mixed-aged, mixed coniferous forests of southwestern Oregon and north-central California. We sampled nocturnal (i.e., primarily foraging) habitat use by 71 radio-tagged spotted owls over 5 yr in 3 study areas and sampled vegetative and physical environmental conditions at inventory plots within 95% utilization distributions of each bird. We compared conditions at available forest patches, represented by the inventory plots, with those at patches used by owls using discrete-choice regressions, the coefficients from which were used to construct exponential resource selection functions (RSFs) for each study area and for all 3 areas combined. Cross-validation testing indicated that the combined RSF was reasonably robust to local variation in habitat availability. The relative probability that a fine-scale patch was selected decreased nonlinearly with distances from nests and streams; varied unimodally with increasing average diameter of coniferous trees and also with increasing basal area of Douglas-fir (Pseudotsuga menziesii) trees; increased linearly with increasing basal areas of sugar pine (Pinus lambertiana) and hardwood trees and with increasing density of understory shrubs. Large-diameter trees (>66 cm) appeared important <400 m from nest sites. The RSF can support comparative risk assessments of the short- versus long-term effects of silvicultural alternatives designed to integrate forest ecosystem restoration and habitat improvement for northern spotted owls. Results suggest fine-scale factors may influence population fitness among spotted owls. © 2011 The Wildlife Society.     

Population fragmentation and major histocompatibility complex variation in the spotted suslik,Spermophilus suslicus

The fragmentation of populations typically enhances depletion of genetic variation, but highly polymorphic major histocompatibility complex (MHC) genes are thought to be under balancing selection and therefore retain polymorphism despite population bottlenecks. In this study, we investigate MHC DRB (class II) exon 2 variation in 14 spotted suslik populations from two regions differing in their degree of habitat fragmentation and gene flow. We found 16 alleles that segregated in a sample of 248 individuals. The alleles were highly divergent and revealed the hallmark signs of positive selection acting on them in the past, showing a significant excess of nonsynonymous substitutions. This excess was concentrated in putative antigen‐binding sites, which suggests that past selection was driven by pathogens. MHC diversity was significantly lower in fragmented western populations than in the eastern populations, characterized by significant gene flow. In contrast to neutral variation, amova did not reveal genetic differentiation between the two regions. This may indicate similar selective pressures shaping MHC variation in both regions until the recent past. However, MHC allelic richness within a population was correlated with that for microsatellites. F_ST outlier analyses have shown that population differentiation at DRB was neither higher nor lower than expected under neutrality. The results suggest that selection on MHC is not strong enough to counteract drift that results from recent fragmentation of spotted suslik populations.     

Microsatellite loci for distinguishing spotted owls (Strix occidentalis), barred owls (Strix varia), and their hybrids

We identified four diagnostic microsatellite loci that distinguish spotted owls (Strix occidentalis), barred owls (Strix varia), F₁ hybrids and backcrosses. Thirty‐four out of 52 loci tested (65.4%) successfully amplified, and four of these loci (11.8%) had allele sizes that did not overlap between spotted and barred owls. The probability of correctly identifying a backcross with these four loci is 0.875. Genotyping potential hybrid owls with these markers revealed that field identifications were often wrong. Given the difficulty of identifying hybrids in the field, these markers will be useful for hybrid identification, law enforcement and spotted owl conservation.     

Development of 37 microsatellite loci for the great gray owl (<Emphasis Type="Italic">Strix nebulosa</Emphasis>) and other <Emphasis Type="Italic">Strix</Emphasis> spp. owls

We developed 37 great gray owl (Strix nebulosa) microsatellite primers from CA and TAGA enriched genomic libraries. Primers were tested in 15 great gray owls from California, USA and Alberta, Canada as well as two other Strix species, spotted owl (S. occidentalis) and barred owl (S. varia). These markers will have broad application in investigations of Strix population structure and genetic diversity.     

The impact of habitat fragmentation on genetic structure of the Japanese sika deer (<Emphasis Type="Italic">Cervus nippon</Emphasis>) in southern Kantoh,revealed by mitochondrial D-loop sequences

In southern Kantoh, Japanese sika deer (Cervus nippon) are distributed discontinuously due to large urban areas and developed road networks. To assess the impact of habitat fragmentation on sika deer subpopulations, we examined mitochondrial D-loop sequences from 435 individuals throughout southern Kantoh. About 13 haplotypes were detected, and their distributions revealed spatial genetic structure. Significant genetic differentiation was observed among seven of eight subpopulations. We found no significant correlation between pairwise F _ST and geographical distance among subpopulations. Genetic diversity indices suggested that seven of eight subpopulations had probably experienced population bottlenecks in the recent past. Therefore, and in the light of the results of a nested clade analysis of these haplotypes, we conclude that recent fluctuations in population size and the interruption of gene flow due to past and present habitat fragmentation have played major roles influencing the spatial genetic structure of the sika deer population. This is the first evidence of spatial genetic population structure in the highly fragmented sika deer population in Honshu, Japan.     

Low genetic variation support bottlenecks in Scandinavian red deer

Loss of genetic variation from genetic drift during population bottlenecks has been shown for many species. Red deer (Cervus elaphus) may have been exposed to bottlenecks due to founder events during postglacial colonisation in the early Holocene and during known population reductions in the eighteenth and nineteenth centuries. In this study, we assess loss of genetic variation in Scandinavian red deer due to potential bottlenecks by comparing microsatellite (n = 14) and mitochondrial DNA variation in the Norwegian and Swedish populations with the Scottish, Lithuanian and Hungarian populations. Bottlenecks are also assessed from the M ratio of populations, heterozygosity excess and from hierarchical Bayesian analyses of their demographic history. Strong genetic drift and differentiation was identified in both Scandinavian populations. Microsatellite variation was lower in both Scandinavian populations compared with the other European populations and mitochondrial DNA variation was especially low in the Swedish population where only one unique haplotype was observed. Loss of microsatellite alleles was demonstrated by low M ratios in all populations except the Hungarian. M ratios’ were especially low in the Scandinavian populations, indicating additional or more severe bottlenecks. Heterozygosity excess compared with the expectation from the number of observed microsatellite alleles suggested a recent bottleneck of low severity in the Norwegian population. Hierarchical Bayesian coalescent analyses consistently yielded estimates of a large ancestral and a small current population size in all investigated European populations and suggested the onset of population decline to be between 5,000 and 10,000 years ago, which coincide well with postglacial colonisation.     

Fine-scale genetic structure in Ethiopian wolves imposed by sociality,migration, and population bottlenecks

We used demographic, spatial, and microsatellite data to assess fine-scale genetic structure in Ethiopian wolves found in the Bale Mountains and evaluated the impact of historical versus recent demographic processes on genetic variation. We applied several analytical methods, assuming equilibrium and nonequilibrium conditions, to assess demography and genetic structure. Genetic variation (H _E = 0.584–0.607, allelic richness = 4.2–4.3) was higher than previously reported for this species and genetic structure was influenced by geography and social structure. Statistically significant F _ST values (0.06–0.08) implied differentiation among subpopulations. STRUCTURE analyses showed that neighbouring packs often have shared co-ancestry and spatial autocorrelation showed higher genetic similarity between individuals within packs and between individuals in neighbouring packs compared to random pairs of individuals. Recent effective population sizes were lower than 2n (where n is the number of packs) and lower than the number of breeding individuals with N _e /N ratios near 0.20. All subpopulations have experienced bottlenecks, one occurring due to a rabies outbreak in 2003. Nevertheless, differentiation among these subpopulations is consistent with long-term migration rates and fragmentation at the end of the Pleistocene. Enhanced drift due to population bottlenecks may be countered by higher migration into disease-affected subpopulations. Contemporary factors such as social structure and population bottlenecks are clearly influencing the level and distribution of genetic variation in this population, which has implications for its conservation.     

Barred owl occupancy surveys within the range of the northern spotted owl

The range expansion by barred owls (Strix varia) into western North America has raised considerable concern regarding their potential effects on declining northern spotted owl (Strix occidentalis caurina) populations, yet most information on the occurrence of barred owls in the region is limited to incidental detections during surveys for spotted owls. To address this shortcoming we investigated response behavior, detection probabilities, and landscape occupancy patterns of barred owls in western Oregon, USA, during conspecific versus spotted owl call-broadcast surveys. Subtle differences in barred owl response behavior to conspecific versus spotted owl vocalizations combined with minor procedural differences between species-specific survey protocols led to a sizeable difference in estimated detection probabilities during conspecific (0.66, 95% CI = 0.61–0.71) versus spotted owl (0.48, 95% CI = 0.39–0.56) surveys. We identified 61 territorial pairs of barred owls during repeated surveys of a multi-ownership study area with the probability of occupancy being highest in the structurally diverse mixture of mature and old forests that occurred almost entirely on public lands. Our findings suggest that research and management strategies to address potential competitive interactions between spotted owls and barred owls will require carefully designed, species-specific survey methods that account for erratic response behaviors and imperfect detection of both species. Our sampling methods can be used by forest managers to determine the occurrence and distribution of barred owls with high confidence. © 2011 The Wildlife Society.     

Site Occupancy Dynamics of Northern Spotted Owls in the Eastern Cascades,Washington, USA, 1990–2003

Abstract: Northern spotted owls (Strix occidentalis caurina) have received intense research and management interest since their listing as a threatened species by the United States Fish and Wildlife Service in 1990. Several spotted owl (Strix occidentalis) response variables have been examined in various investigations, but recent advances in statistical modeling permit evaluations of temporal and spatial variability in site occupancy, local-extinction, and colonization probabilities while incorporating imperfect detection probabilities. Following recent work by other researchers on site occupancy dynamics of spotted owls in Oregon, USA, we evaluated temporal variability of detection, occupancy, local-extinction, and colonization probabilities for spotted owls, as well as potential influences of barred owl (Strix varia) presence on these parameters. We used spotted owl survey data collected from 1990 to 2003 on a study area in the eastern Cascades Mountains, Washington, USA, to compare competing occupancy models from Program PRESENCE using Akaike's Information Criterion. Detection probabilities for individual spotted owls ranged from 0.54 to 0.80 if barred owls were not detected during the survey season and from 0.19 to 0.71 if barred owls were detected during the survey season. Pair detection probabilities ranged from 0.27 to 0.67 if barred owls were not detected during an individual survey and from 0.09 to 0.36 if barred owls were detected during an individual survey. During the study, site occupancy probabilities for spotted owl pairs declined by approximately 50%. For all spotted owls, both singles and pairs, site occupancy probabilities declined moderately during the study. Barred owl presence was negatively associated with spotted owl detection probabilities, and it had a positive association with local-extinction probabilities for all spotted owls, both singles and pairs. Given that our study area has supported higher densities of barred owls for longer periods than other study areas, our results may provide insight into how barred owls have influenced spotted owl site occupancy dynamics in adjacent British Columbia, Canada, or will influence spotted owl site occupancy dynamics in Oregon and California, USA, in the future.     

Evidence for a recent genetic bottleneck in the endangered Florida Keys silver rice rat (<Emphasis Type="Italic">Oryzomys argentatus</Emphasis>) revealed by microsatellite DNA analyses

Low levels of genetic variation are thought to contribute significantly to the higher extinction rates of endemic island populations compared to their mainland counterparts. We used six microsatellite loci to compare the genetic structure of the endangered silver rice rat (Oryzomys argentatus) population in Saddlebunch Key, Florida to the mainland population of the closely related marsh rice rat (Oryzomys palustris natator) in Everglades National Park. Allelic richness and gene diversity are significantly lower in Saddlebunch Key than in the larger mainland population, and the two populations are significantly differentiated as measured by both F-statistics and Bayesian clustering methods. These findings support the classification of the Keys population as a “distinct vertebrate population” by the U.S. Fish and Wildlife Service. Current gene diversity (H _E) is higher than expected under mutation-drift equilibrium in Saddlebunch Key, indicating a genetic bottleneck. The Keys population also exhibits a mode shift in its allele frequency distribution which suggests a very recent bottleneck has occurred and is consistent with reports of recent population declines. Although habitat loss and exotic species pose a more immediate and serious threat to silver rice rats, the continued loss of genetic variation may contribute to their long-term extinction risk due to inbreeding or by lowering the population’s ability to adapt to future environmental changes. The protection of habitat and the removal of introduced predators and competitors may help increase the population size of silver rice rats and lower their risk of extinction, both from a demographic and a genetic perspective.     

Genetic diversity in adult and seedling populations of <Emphasis Type="Italic">Primula vulgaris</Emphasis> in a fragmented agricultural landscape

Habitat fragmentation is known to generally reduce the size of plant populations and increase their isolation, leading to genetic erosion and increased between-population genetic differentiation. In Flanders (northern Belgium) Primula vulgaris is very rare and declining. Populations have incurred strong fragmentation for the last decades and are now restricted to a few highly fragmented areas in an intensively used agricultural landscape. Previous studies showed that small populations of this long-lived perennial herb still maintained high levels of genetic variation and low genetic differentiation. This pattern can either indicate recent gene flow or represent historical variation. Therefore, we used polymorphic microsatellite loci to investigate genetic variation and structure in adult (which may still reflect historical variation) and seedling (recent generation, thus affected by current processes) life stages. The recent generation (seedlings) showed a significant loss of observed heterozygosity (H _o) together with lower expected heterozygosity (H _e), a trend for higher inbreeding levels (F _IS) and higher differentiation (F _ST) between populations compared to the adult generation. This might result from (1) a reduction in effective population size, (2) higher inbreeding levels in the seedlings, (3) a higher survival of heterozygotes over time due to a higher fitness of heterozygotes (heterosis) and/or a lower fitness of homozygotes (inbreeding depression), (4) overlapping generations in the adult life stage, or (5) a lack of establishment of new (inbred) adults from seedlings due to degraded habitat conditions. Combining restoration of both habitat quality and gene flow between populations may be indispensable to ensure a sustainable conservation of fragmented populations.     

Genetic analysis of four wild chum salmon<Emphasis Type="Italic">Oncorhynchus keta</Emphasis> populations in China based on microsatellite markers

Synopsis To assess the genetic variation and population structure of wild chum salmon in China, we analyzed microsatellite loci for populations in the Amur, Wusuli, Suifen Current and the Tumen rivers. We evaluated expected heterozygosity with two estimators of genetic differentiation (F_ST and G_ST) and Nei’s standard genetic distance. The average expected heterozygosity across the 10 loci was 0.65 in the Wusuli River and the Suifen Current River, 0.64 in the Amur River and 0.66 in the Tumen River, The results of this study show that the recent declines in chum salmon have not led to low levels of genetic variability in China. The proportion of inter-population subdivision among chum salmon was between 5.7 and 6.8%. According to the estimator used, the NJ tree based on Nei’s standard genetic distance indicated that there were two different branches (the Sea of Okhotsk branch and the Sea of Japan branch), the Amur River and the Wusuli River populations were closer, while the Suifen Current River and the Tumen River clustered together. The genetic test for population bottlenecks provided no evidence for a significant genetic signature of population decline, which is consistent with the record of the four populations we have in the last few years.     

Genetic rescue of an inbred captive population of the critically endangered Puerto Rican crested toad (<Emphasis Type="Italic">Peltophryne lemur</Emphasis>) by mixing lineages

The Puerto Rican crested toad (Peltophryne lemur) is currently composed of a single wild population on the south coast of Puerto Rico and two captive populations founded by animals from the northern and southern coasts. The main factors contributing to its decline are habitat loss, inundation of breeding ponds during storms, and impacts of invasive species. Recovery efforts have been extensive, involving captive breeding and reintroductions, habitat restoration, construction of breeding ponds, and public education. To guide future conservation efforts, genetic variation and differentiation were assessed for the two captive colonies and the remaining wild population using the mitochondrial control region and six novel microsatellite loci. Only two moderately divergent mitochondrial haplotypes were found, with one fixed in each of the southern and northern lineages. Moderate genetic variation exists for microsatellite loci in all three groups. The captive southern population has not diverged substantially from the wild population at microsatellite loci (F _ST = 0.03), whereas there is little allelic overlap between the northern and southern lineages at five of six loci (F _ST > 0.3). Despite this differentiation, they are no more divergent than many populations of other amphibian species. As the northern breeding colony may not remain viable due to its small size and inbred nature, it is recommended that a third breeding colony be established in which northern and southern individuals are combined. This will preserve any northern adaptive traits that may exist, and provide animals for release in the event that the pure northern lineage becomes extirpated.     

Genetic variation in two land snails, Cepaea nemoralis and Succinea putris (Gastropoda, Pulmonata), from sites differing in heavy metal content

Allozyme variation was determined in two land snail species (Cepaea nemoralis and Succinea putris) from four localities in northern Belgium. In each locality we selected a polluted and a nearby, less-polluted, reference plot. We examined whether (i) genetic variability differed between the polluted and reference plots, (ii) populations from polluted plots experienced recent bottlenecks, and (iii) certain allele or genotype frequencies were associated with the pollution. Our results suggest that (i) about 13% of the genetic differentiation in C. nemoralis and 5% in S. putris was due to differences among polluted and reference plots, (ii) polluted and reference plots had comparable levels of genetic variation, but in C. nemoralis observed heterozygosities were higher in polluted plots, (iii) most plots showed significant evidence for recent bottlenecks, irrespective of the degree of pollution, so that bottlenecks seem poor indicators of pollution-induced stress in land snails, and (iv) mutagenic or pollution-induced modifications did not seem to account for new allozyme variants in polluted sites. The observed patterns of genetic variation may be explained by the action of genetic drift, pollution-mediated selection, restricted gene flow, or a combination of these processes.     

Habitat Use and Selection by California Spotted Owls in a Postfire Landscape

ABSTRACT Forest fire is often considered a primary threat to California spotted owls (Strix occidentalis occidentalis) because fire has the potential to rapidly alter owl habitat. We examined effects of fire on 7 radiomarked California spotted owls from 4 territories by quantifying use of habitat for nesting, roosting, and foraging according to severity of burn in and near a 610-km²fire in the southern Sierra Nevada, California, USA, 4 years after fire. Three nests were located in mixed-conifer forests, 2 in areas of moderate-severity burn, and one in an area of low-severity burn, and one nest was located in an unburned area of mixed-conifer-hardwood forest. For roosting during the breeding season, spotted owls selected low-severity burned forest and avoided moderate- and high-severity burned areas; unburned forest was used in proportion with availability. Within 1 km of the center of their foraging areas, spotted owls selected all severities of burned forest and avoided unburned forest. Beyond 1.5 km, there were no discernable differences in use patterns among burn severities. Most owls foraged in high-severity burned forest more than in all other burn categories; high-severity burned forests had greater basal area of snags and higher shrub and herbaceous cover, parameters thought to be associated with increased abundance or accessibility of prey. We recommend that burned forests within 1.5 km of nests or roosts of California spotted owls not be salvage-logged until long-term effects of fire on spotted owls and their prey are understood more fully.