Detecting and quantifying introgression in hybridized populations: simplifying assumptions yield overconfidence and uncertainty

A growing threat to the conservation of many native species worldwide is genetic introgression from non‐native species. Although improved molecular genetic techniques are increasing the availability of species‐diagnostic markers for many species, efficient field sampling design and reliable data interpretation require accurate estimates of uncertainty associated with the detection of non‐native alleles and the quantification of introgression in native populations. Using fish populations as examples, we developed a simulation model of an age‐structured population that tracks the introduction and inheritance of non‐native alleles across generations by simulating stochastic mating and survival of individual fish and the resulting transmission of diagnostic markers. To simulate detection and quantification of introgression, we sampled varying combinations of n fish and m diagnostic markers to detect and quantify introgression from thousands of virtual, independent fish populations for a wide range of hybridization scenarios. Using the results of simulated sampling, we quantified the extent to which common simplifying assumptions regarding population structure and inheritance mechanisms can lead to the following: (i) overconfidence in our ability to detect non‐native alleles and (ii) unrealistically narrow confidence intervals for estimates of the proportion of non‐native alleles present. Under many circumstances, commonly used simplifying assumptions underestimate the probability of failing to detect ongoing introgression and the uncertainty associated with estimates of introgression by orders of magnitude. Such overconfidence in our ability to detect and quantify introgression can affect critical conservation and management decisions regarding native species undergoing or at risk of introgression from non‐native species.     

Evaluation of strategies to conserve and restore intraspecific biodiversity of brown trout: outcomes from genetic monitoring in the French Alps

Introduction of nonnative cultured fish is one of the most important threats to native salmonid populations. In brown trout, more than a century of stocking practices has led to a large hybridization between initially geographically isolated lineages, threatening native populations and thereby intraspecific diversity. In the French region of Haute-Savoie, managers and scientists implemented together three management strategies (genetic refuge, direct translocation of wild spawners and stocking with native fry) on 19 test sites for more than 15 years, in the aim to recover pure or nearly pure native populations. Here we propose an assessment of the different management strategies based on a synthetic analysis of the evolution of the introgression rate. While none of the implemented strategies completely achieves the initial objective to restore pure native populations, they differ in their efficiency: introgression rates tend to decrease quickly when direct translocation of native spawners of stocking with native fry strategies are used. The genetic refuge strategy shows slower and more heterogeneous changes of introgression rates. In general, pure nonnative fish are efficiently removed but at the cost of an increased presence of hybrids. Our results imply that intraspecific dynamics react quickly to management practices and that these changes are probably fueled by evolutionary feedbacks that are not yet well understood.     

Determinants of hierarchical genetic structure in Atlantic salmon populations: environmental factors vs. anthropogenic influences

Disentangling the effects of natural environmental features and anthropogenic factors on the genetic structure of endangered populations is an important challenge for conservation biology. Here, we investigated the combined influences of major environmental features and stocking with non‐native fish on the genetic structure and local adaptation of Atlantic salmon (Salmo salar) populations. We used 17 microsatellite loci to genotype 975 individuals originating from 34 French rivers. Bayesian analyses revealed a hierarchical genetic structure into five geographically distinct clusters. Coastal distance, geological substrate and river length were strong predictors of population structure. Gene flow was higher among rivers with similar geologies, suggesting local adaptation to geological substrate. The effect of river length was mainly owing to one highly differentiated population that has the farthest spawning grounds off the river mouth (up to 900 km) and the largest fish, suggesting local adaptation to river length. We detected high levels of admixture in stocked populations but also in neighbouring ones, implying large‐scale impacts of stocking through dispersal of non‐native individuals. However, we found relatively few admixed individuals suggesting a lower fitness of stocked fish and/or some reproductive isolation between wild and stocked individuals. When excluding stocked populations, genetic structure increased as did its correlation with environmental factors. This study overall indicates that geological substrate and river length are major environmental factors influencing gene flow and potential local adaptation among Atlantic salmon populations but that stocking with non‐native individuals may ultimately disrupt these natural patterns of gene flow among locally adapted populations.     

Evidence for selective angling of introduced trout and their hybrids in a stocked brown trout population

Comparisons of the genetic composition of brown trout Salmo trutta captured by anglers and by electrofishing based on three diagnostic microsatellite loci provided strong evidence that angling is selective in a stocked brown trout population. At two sites, anglers caught significantly younger trout and proportionally more introduced hatchery trout and hybrids than were observed in electrofishing surveys. Selective angling, in combination with a small legal catch size, may have considerably eliminated introduced trout and hybrids before spawning at the study sites, and thus may have reduced the introgression of alien genes into the local gene pool. Angling can be an important factor influencing the genetic structure of fish populations and should be taken into account in studies of introgressive hybridization in stocked fish populations and their management. In this study, demographic consequences of stocking were not assessed. Thus, even though the genetic consequences of stocking may be minimal or largely reversible through angling, resource competition between native and introduced trout, until they reach legal catch size, is expected to have a negative effect on the productivity of the indigenous trout population.     

A genetically distinct wild redband trout (<Emphasis Type="Italic">Oncorhynchus mykiss gairdneri</Emphasis>) population in Crane Prairie Reservoir,Oregon, persists despite extensive stocking of hatchery rainbow trout (<Emphasis Type="Italic">O. m. irideus</Emphasis>)

Crane Prairie Reservoir in the upper Deschutes River Basin has historically supported a wild population of migratory Deschutes River redband trout. Owing to its status as a premier destination for recreational angling in Oregon, the reservoir has been stocked with domesticated hatchery rainbow trout since 1955. In recent years the wild redband trout population has experienced a substantial decline. Effects on productivity related to genetic interaction with naturally spawning hatchery-origin fish (fitness risks) have not been determined. The species Oncorhynchus mykiss has been characterized with substantial genetic diversity throughout the Deschutes River Basin that further heightens the challenge of identifying specific conservation needs of wild populations. A conservation plan for Crane Prairie wild redband trout requires a better understanding of the natural reproductive success of out-of-basin hatchery trout in the reservoir tributaries, and the similarity between Crane Prairie redband trout with other extant redband trout populations in the basin. Using a suite of 17 microsatellite nuclear DNA markers, we evaluated the genetic structure among Crane Prairie Reservoir redband trout, hatchery rainbow trout, and two adjacent populations of redband trout from within the Upper Deschutes River Basin. We observed significant heterogeneity between the hatchery and wild Crane Prairie populations that may reflect differences in life histories, differential productivity and assortative mating. The genetic distinctions observed among the three redband trout populations suggest restricted gene flow and genetic drift within the upper basin. Temporally stratified sampling and larger numbers of samples will be necessary to confirm these conclusions.     

Timing is everything: Fishing‐season placement may represent the most important angling‐induced evolutionary pressure on Atlantic salmon populations

Fisheries‐induced evolution can change the trajectory of wild fish populations by selectively targeting certain phenotypes. For important fish species like Atlantic salmon, this could have large implications for their conservation and management. Most salmon rivers are managed by specifying an angling season of predetermined length based on population demography, which is typically established from catch statistics. Given the circularity of using catch statistics to estimate demographic parameters, it may be difficult to quantify the selective nature of angling and its evolutionary impact. In the River Etne in Norway, a recently installed trap permits daily sampling of fish entering the river, some of which are subsequently captured by anglers upstream. Here, we used 31 microsatellites to establish an individual DNA profile for salmon entering the trap, and for many of those subsequently captured by anglers. These data permitted us to investigate time of rod capture relative to river entry, potential body size‐selective harvest, and environmental variables associated with river entry. Larger, older fish entered the river earlier than smaller, younger fish of both sexes, and larger, older females were more abundant than males and vice versa. There was good agreement between the sizes of fish harvested by angling, and the size distribution of the population sampled on the trap. These results demonstrate that at least in this river, and with the current timing of the season, the angling catch reflects the population's demographics and there is no evidence of size‐selective harvest. We also demonstrated that the probability of being caught by angling declines quickly after river entry. Collectively, these data indicate that that the timing of the fishing season, in relation to the upstream migration patterns of the different demographics of the population, likely represents the most significant directional evolutionary force imposed by angling.     

Genetic diversity and population structure of the northern snakehead (<Emphasis Type="Italic">Channa argus</Emphasis> Channidae: Teleostei) in central China: implications for conservation and management

Major threats to freshwater fish diversity now include loss of native genetic diversity as a consequence of translocations of fishes between sites and from hatcheries to sites, and small effective population sizes resulting from overfishing and/or habitat loss. Ten polymorphic microsatellite markers were employed to evaluate genetic diversity, population genetic structure and gene flow amongst nine populations of the ecologically and economically important fish, the northern snakehead (Channa argus), in three river systems in central China. Multiple analyses revealed evidence of high genetic diversity and pronounced subdivision based on both regional separation and on river systems. A lack of evidence of genetic bottleneck over recent generations was consistent with the long-term stability of population size and contemporary distribution. The effective population sizes for most C. argus populations were small, suggesting the need for future conservation efforts focusing on these populations. Different lines of evidence point to the local enhancement of stocks by both aquaculture-reared fish and the transfer of wild fish. This study illustrates how human activities may affect genetic diversity and population genetic structure of C. argus populations, and highlights the need for new management regimes to protect native freshwater fish genetic diversity.     

Characterizing genetic integrity of rear-edge trout populations in the southern Appalachians

Vertebrate populations at the periphery of their range can show pronounced genetic drift and isolation, and therefore offer unique challenges for conservation and management. These populations are often candidates for management actions such as translocations that are designed to improve demographic and genetic integrity. This is particularly true of coldwater species like brook trout (Salvelinus fontinalis), whose numbers have declined greatly across its historic range. At the southern margin, remnant wild populations persist in isolated headwater streams, and many have a history of receiving translocated individuals through either stocking of hatchery reared fish, relocation of wild fish, or both during restoration attempts. To determine current genetic integrity and resolve the genetic effects of past management actions for brook trout populations in SC, USA, we genetically assessed all 18 documented remaining brook trout populations along with individuals acquired from six hatcheries with recorded stocking events in SC. Our results indicated that six of the 18 streams showed signs of hatchery admixture (range 57–97%) and restored patches retained genetic signatures from multiple source populations. Populations had among the lowest genetic diversity (min average H_E?=?0.147) and effective number of breeders (mean N_b?=?31.2) estimates observed throughout the native brook trout range. Populations were highly differentiated (mean pair-wise F_ST?=?0.396), and substantial genetic divergence was evident across major river drainages (max pair-wise F_ST?=?0.773). The lowest local genetic diversity and highest genetic differentiation ever reported for this species make its conservation a challenging task, particularly when combined with other threats such as climate change and non-native species. We offer recommendations on managing peripheral populations with depleted genetic characteristics and provide a reference for determining which existing populations will best serve as sources for future translocation efforts aimed at enhancing or restoring wild brook trout genetic integrity.     

Evidence of two contrasting brown trout Salmo trutta populations spatially separated in the River Borne (France) and shift in management towards conservation of the native lineage

A multidisciplinary study was made of brown trout Salmo trutta in the Borne River, a typical fast-flowing mountain stream in the Northern French Alps, in the geographical range of the Mediterranean lineages (ML). Information on (1) the proportion of stocked fluoro-marked fish in the angling harvest, (2) the introgression of introduced DNA microsatellite alleles into the native gene pool and (3) the demography of the population in situ in autumn revealed two contrasting populations separated by a physical barrier to upstream migration. A native S. trutta population ( c . 10 000 adults) lives downstream of the barrier and is characterized by a large frequency of ML alleles (82–97%) and high densities (43–55 fish 100 m⁻²). This population is maintained predominantly by natural recruitment of juveniles (51–82%). In contrast, the upstream population is characterized by a large frequency of Atlantic lineage (AL) alleles (78–100%) and low densities (1–2 fish 100 m⁻²) and appears to be maintained by restocking (90–100%). The origins of these sharply contrasting populations appear to reflect isolation by an impassable barrier, catastrophic flooding, a downstream gradient in water quality, stocking and fishing pressure. The native downstream population has been resilient to large sudden floods and to intensive stockings of domesticated AL fish. The results of this study justify a shift in management towards conservation and rehabilitation of the native population.     

Breakdown of the brown trout evolutionary history due to hybridization between native and cultivated fish

Genetic changes in the population structure of brown trout Salmo trutta in the eastern Pyrenees were monitored during the 1990s. Stocking with cultivated exogenous fish has resulted in introgressed populations where those with higher introgression coefficients also have the highest values of heterozygosity. Nevertheless, this increase of local diversity reflects a decrease of genetic differentiation between populations and loss of native alleles. These changes obscure native gene pools and modify evolutionary distinctions among native brown trout populations.     

Widespread hybridization in the introduced hog deer population of Victoria,Australia, and its implications for conservation

In Australia, many species have been introduced that have since undergone drastic declines in their native range. One species of note is the hog deer (Axis porcinus) which was introduced in the 1860s to Victoria, Australia, and has since become endangered in its native range throughout South‐East Asia. There is increased interest in using non‐native populations as a source for genetic rescue; however, considerations need to be made of the genetic suitability of the non‐native population. Three mitochondrial markers and two nuclear markers were sequenced to assess the genetic variation of the Victorian population of hog deer, which identified that the Victorian population has hybrid origins with the closely related chital (Axis axis), a species that is no longer present in the wild in Victoria. In addition, the mitochondrial D‐loop region within the Victorian hog deer is monomorphic, demonstrating that mitochondrial genetic diversity is very low within this population. This study is the first to report of long‐term persistence of hog deer and chital hybrids in a wild setting, and the continual survival of this population suggests that hybrids of these two species are fertile. Despite the newly discovered hybrid status in Victorian hog deer, this population may still be beneficial for future translocations within the native range. However, more in‐depth analysis of genetic diversity within the Victorian hog deer population and investigation of hybridization rates within the native range are necessary before translocations are attempted.     

Disentangling stocking introgression and natural migration in brown trout: survival success and recruitment failure in populations with semi‐supportive breeding

1. Introgression into natural salmonid populations from stocked conspecifics has been widely studied. Outcomes vary from no effect even after decades of stocking, to population replacement after only a couple of generations. Potential introgression caused by semi‐supportive breeding (i.e. using a mixture of local strains as brood stock) is, however, less well studied. 2. We investigated population structure of brown trout (Salmo trutta) in a regulated alpine lake with three natural, environmentally contrasting tributaries used as spawning and rearing habitat. Massive semi‐supportive breeding of admixed local strains has been implemented for decades. Stocked trout represented c. 17% of the total lake population, and a substantial post‐release survival reflects a considerable potential for introgression. However, the mark‐recapture studies indicate no spawning runs of stocked fish. 3. Using 13 polymorphic microsatellite loci, we found natural straying and non‐native reproduction, especially among wild populations inhabiting environmentally unstable habitat. Retained genetic structure across tributaries indicated low reproductive success of wild‐born non‐natives. Moreover, the genetic structure among tributaries has probably not been influenced by semi‐supportive breeding, because of recruitment failure of stocked trout.     

Estimating the long-term effects of stocking domesticated trout into wild brown trout (Salmo trutta) populations: an approach using microsatellite DNA analysis of historical and contemporary samples

Indigenous salmonid fish gene pools are affected by domesticated conspecifics, derived from aquaculture escapes and deliberate releases. Variability was examined at nine microsatellite loci in order to assess the long-term impact of stocking domesticated trout in two brown trout populations. The study was based on analysis of two historical samples (1945-56), represented by old scale collections, and seven contemporary samples (1986-2000). In one population historical and contemporary samples were remarkably genetically similar despite more than a decade of intense stocking. Estimation of admixture proportions showed a small genetic contribution from domesticated trout (approximately 6%), and individual admixture analysis demonstrated a majority of nonadmixed individuals. The expected genetic contribution by domesticated trout was 64%, assessed from the number of stocked trout and assuming equal survival and reproductive performance of wild and domesticated trout. This demonstrates poor performance and low fitness of domesticated trout in the wild. In another population there was a strong genetic contribution from domesticated trout (between 57% and 88% in different samples), both in samples from a broodstock thought to represent the indigenous population and in a sample of wild spawners. Survival of domesticated trout and admixture with indigenous fish in the broodstock and subsequent stocking into the river, combined with a low population size of native trout relative to the number of stocked trout, could explain the observed introgression. Few nonadmixed individuals remained in the introgressed population, and I discuss how individual admixture analysis can be used to identify and conserve nonintrogressed remains of the population.     

Loss of genetic integrity correlates with stocking intensity in brook charr (Salvelinus fontinalis)

Supportive breeding and stocking performed with non‐native or domesticated fish to support sport fishery industry is a common practice throughout the world. Such practices are likely to modify the genetic integrity of natural populations depending on the extent of genetic differences between domesticated and wild fish and on the intensity of stocking. The purpose of this study is to assess the effects of variable stocking intensities on patterns of genetic diversity and population differentiation among nearly 2000 brook charr (Salvelinus fontinalis) from 24 lakes located in two wildlife reserves in Québec, Canada. Our results indicated that the level of genetic diversity was increased in more intensively stocked lakes, mainly due to the introduction of new alleles of domestic origin. As a consequence, the population genetic structure was strongly homogenized by intense stocking. Heavily stocked lakes presented higher admixture levels and lower levels of among lakes genetic differentiation than moderately and un‐stocked lakes. Moreover, the number of stocking events explained the observed pattern of population genetic structure as much as hydrographical connections among lakes in each reserve. We discuss the implications for the conservation of exploited fish populations and the management of stocking practices.     

Allozyme diversity in brown trout (Salmo trutta) from Central Spain: Genetic consequences of restocking

1.  The brown trout ( Salmo trutta ) represents one of the main freshwater resources in Spain, but habitat alterations and overharvesting have contributed to the decline or disappearance of numerous natural populations. In addition, reinforcement programs of wild populations based on releases of hatchery reared fish of exogenous origin compromise the conservation of remnant native trout resources.
2.  We present allozymic data from Central Spain trout populations including stocked and unstocked populations. Although the levels of genetic variation observed were low and affected by hatchery releases (p = 18.23%, Ho= 3.39%), they were within the range observed in other European areas.
3.  The effective introduction of hatchery reared fish is genetically homogenising the populations in the studied area and disturbing the ancestral pattern of genetic variation that distinguishes the Tajo and Duero basins. Within the eight natural populations analysed, seven had alleles assigned to the foreign trout. The introgression in these populations, following the LDH-5 * 90 allele frequency, ranged between 2% and 29.4%, but those values are not in concordance with the respective stocking effort undertaken in each population. Moreover, the release of hatchery-reared fish does not solve the problems related to the reduced size of wild populations and their recruitment instability.     

The effects of fisheries management on harvest rates of native and non-native salmonid fish species

In central Europe, both brown trout Salmo trutta and European grayling Thymallus thymallus are threatened native salmonid species with high value in recreational angling and nature conservation. On the other hand, rainbow trout Oncorhynchus mykiss and brook trout Salvelinus fontinalis are intensively stocked non-native species of high angling value but no value for nature conservation. This study tested if harvest rates of native salmonids are negatively correlated to intensive stocking and harvest rates of non-native salmonids in inland freshwater recreational fisheries. Data were collected from 250 fishing sites (river and stream stretches) over 13 years using mandatory angling logbooks. Logbooks were collected from individual anglers by the Czech Fishing Union in the regions of Prague and Central Bohemia, Czechia (central Europe) and processed by the author of this study. In result, anglers harvested 200,000 salmonids with total weight of 80 tons over 13 years. Intensive stocking of multiple salmonid species lead to slightly lower harvests of native salmonids. Inversely, intensive harvests of multiple salmonid species lead to slightly higher harvest of native salmonids. Recapture rates of stocked salmonids were relatively low (0.6%–3.7%), proving fish stocking moderately ineffective. Since the effects of non-native salmonid stocking and harvest rates on native salmonid harvest were significant but not strong, it is suggested that rivers and streams that support fishing for non-native salmonids still support fishing for native salmonids. However, this idea does not apply for fishing sites with really high intensity of non-native salmonid stocking – harvest rates of natives were very low on these fishing sites.     

Strategies for the conservation and management of isolated salmonid populations: lessons from Japanese streams

1. Endangered native populations of stream salmonids in Japan face three major threats: (i) negative interactions with introduced hatchery‐reared fish, (ii) fragmentation of habitat by impassable dams and (iii) recreational angling. 2. To prevent imminent extinction of many local populations, we evaluated these threats and possible conservation actions for red‐spotted masu salmon (Oncorhynchus masou ishikawae) and white‐spotted charr (Salvelinus leucomaenis japonicus) in the Fuji River system in central Japan. 3. Red‐spotted masu salmon and white‐spotted charr occupied only 0.73 and 2.4% of suitable thermal habitats, respectively, with masu salmon typically occupying habitats closer to human population centres. 4. Population viability analysis resulted in a 100‐year probability of extinction of 78.1% for masu salmon and 48.1% for charr. However, extinction risk of both species was predicted to be <5% if the carrying capacity increased from 141 to 303 for masu salmon and from 94 to 125 for charr, by allowing fish passage at the lower end of the habitat, and if annual adult survival rate increased by 0.04. Adult survival rate was the principal factor associated with population persistence. 5. To conserve isolated populations of stream‐dwelling salmonids, we recommend (i) assessing the distribution of remnant native and non‐native fish populations, (ii) that fishing regulations are modified to improve adult survival and population persistence and (iii) that fragmented reaches be reconnected to adjacent habitat, for example by removing or modifying artificial barriers to increase the carrying capacity of the isolated populations. Reconnection of fragmented reaches should, however, be avoided if it results in non‐native fish invading isolated populations.     

Population genetic structure after 125 years of stocking in sea trout (<Emphasis Type="Italic">Salmo trutta</Emphasis> L.)

Stocking can be an effective management and conservation tool, but it also carries the danger of eroding natural population structure, introducing non-native strains and reducing genetic diversity. Sea trout, the anadromous form of the brown trout (Salmo trutta), is a highly targeted species that is often managed by stocking. Here, we assess the present-day population genetic structure of sea trout in a backdrop of 125 years of stocking in Northern Germany. The study area is characterized by short distances between the Baltic and North Sea river watersheds, historic use of fish from both watersheds for stocking, and the creation of a potential migration corridor between the Baltic and North Sea with the opening of the Kiel Canal 120 years ago. A survey of 24 river systems with 180 SNPs indicates that moderate but highly significant population genetic structure has persisted both within and between the Baltic and North Sea. This genetic structure is characterized by (i) heterogeneous patterns of admixture between the Baltic and North Sea that do not correlate with distance from the Kiel Canal and are therefore likely due to historic stocking practises, (ii) genetic isolation by distance in the Baltic Sea at a spatial scale of <?200 km that is consistent with the homing behaviour of sea trout, and (iii) at least one genetically distinct Baltic Sea river system. In light of these results, we recommend keeping fish of North Sea and Baltic Sea origin separate for stocking, and restricting Baltic Sea translocations to neighbouring river systems.     

Non‐native trout limit native brook trout access to space and thermal refugia in a restored large‐river system

We used direct observation via snorkeling surveys to quantify microhabitat use by native brook (Salvelinus fontinalis) and non‐native brown (Salmo trutta) and rainbow (Onchorynchus mykiss) trout occupying natural and restored pool habitats within a large, high‐elevation Appalachian river, United States. Permutational multivariate analysis of variance (PERMANOVA) and subsequent two‐way analysis of variance (ANOVA) indicated a significant difference in microhabitat use by brook and non‐native trout within restored pools. We also detected a significant difference in microhabitat use by brook trout occupying pools in allopatry versus those occupying pools in sympatry with non‐native trout—a pattern that appears to be modulated by size. Smaller brook trout often occupied pools in the absence of non‐native species, where they used shallower and faster focal habitats. Larger brook trout occupied pools with, and utilized similar focal habitats (i.e. deeper, slower velocity) as, non‐native trout. Non‐native trout consistently occupied more thermally suitable microhabitats closer to cover as compared to brook trout, including the use of thermal refugia (i.e. ambient–focal temperature >2°C). These results suggest that non‐native trout influence brook trout use of restored habitats by: (1) displacing smaller brook trout from restored pools, and (2) displacing small and large brook trout from optimal microhabitats (cooler, deeper, and lower velocity). Consequently, benefits of habitat restoration in large rivers may only be fully realized by brook trout in the absence of non‐native species. Future research within this and other large river systems should characterize brook trout response to stream restoration following removal of non‐native species.     

Hybridisation in European ungulates: an overview of the current status,causes, and consequences

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