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The expression of anadromy in partially migratory salmonid populations is influenced by sex-specific interactions among an individual’s genotype, condition, and environment, but genotype–phenotype relationships prior to the expression of migratory type are poorly understood. We examined whether juvenile growth and condition differed with respect to sex and a migration-associated genomic region (Omy05) in a coastal California population of steelhead and rainbow trout (Oncorhynchus mykiss). Sex and Omy05 genotype had additive effects on annual growth from age 0+ to age 1+ (∼6–18 months old), with higher growth in males and individuals with copies of the rearranged–resident haplotype. Condition at age 1+ increased with the number of copies of the rearranged–resident haplotype, with similar support for additive or interactive effects with sex; additive effects suggested that genotype differences occurred in both sexes and also that condition was slightly higher in males, while interactive effects suggested that the genotype differences occurred only in males. Our results indicate that phenotypic differences related to sex and Omy05 genotype occur well in advance of anadromous migration or freshwater maturation in this southern O. mykiss population.

Unexpectedly simple Chinook salmon are known to return to spawn at two distinct times of the year: spring and fall. Individuals that return during these times have generally been referred to as parts of distinct groups, or ecotypes, with traits specific to their timing and presumed divergence being caused by the lack of interbreeding. By looking at genomes across fish from both runs, Thompson et al. found that a single genomic region of interest was nearly perfectly associated with run timing but not with other traits such as maturity and fat reserves (see the Perspective by McKinney). Further, they conclude that the region operates as a Mendelian trait, with assortment dictating run timing and associated phenotypes being caused by the migration environment rather than genetics. Science , this issue p. 609 ; see also p. 526

Males and females often differ in their fitness optima for shared traits that have a shared genetic basis, leading to sexual conflict. Morphologically differentiated sex chromosomes can resolve this conflict and protect sexually antagonistic variation, but they accumulate deleterious mutations. However, how sexual conflict is resolved in species that lack differentiated sex chromosomes is largely unknown. Here we present a chromosome-anchored genome assembly for rainbow trout (Oncorhynchus mykiss) and characterize a 55-Mb double-inversion supergene that mediates sex-specific migratory tendency through sex-dependent dominance reversal, an alternative mechanism for resolving sexual conflict. The double inversion contains key photosensory, circadian rhythm, adiposity and sex-related genes and displays a latitudinal frequency cline, indicating environmentally dependent selection. Our results show sex-dependent dominance reversal across a large autosomal supergene, a mechanism for sexual conflict resolution capable of protecting sexually antagonistic variation while avoiding the homozygous lethality and deleterious mutations associated with typical heteromorphic sex chromosomes.

Whole-genome duplications (WGDs) have occurred repeatedly and broadly throughout the evolutionary history of eukaryotes. However, the effects of WGD on genome function and evolution remain unclear. The salmonid WGD that occurred approximately 88 million years ago presents an excellent opportunity for studying the effects of WGD as ∼10–15% of each salmonid genome still exhibits tetrasomic inheritance. Herein, we utilized the rainbow trout (Oncorhynchus mykiss) genome assembly and brain transcriptome data to examine the fate of gene pairs (ohnologs) following the salmonid whole-genome duplication. We find higher sequence identity between ohnologs located within known tetrasomic regions than between ohnologs found in disomic regions, and that tetrasomically inherited ohnologs showed greater similarity in patterns of gene expression and per ohnolog were lower expressed, than disomically inherited ohnologs. Enrichment testing for Gene Ontology terms identified 49 over-represented terms in tetrasomically inherited ohnologs compared to disomic ohnologs. However, why these ohnologs are retained as tetrasomic is difficult to answer. It could be that we have identified salmonid specific “dangerous duplicates”, that is, genes that cannot take on new roles following WGD. Alternatively, there may be adaptive advantages for retaining genes as functional duplicates in tetrasomic regions, as presumably, movement of these genes into disomic regions would affect both their sequence identity and their gene expression patterns.

The construction of dams and water diversions has severely limited access to spawning habitat for anadromous fishes. To mitigate for these impacts, hatchery programs rear and release millions of juvenile salmonids, including steelhead, the anadromous ecotype of the species Oncorhynchus mykiss. These programs sometimes use nonindigenous broodstock sources that may have negative effects on wild populations. In California, however, only one anadromous fish hatchery program currently uses nonnative broodstock: the steelhead program at Nimbus Fish Hatchery on the American River, a tributary of the Sacramento River in the California Central Valley. The goal of this study was to determine if potentially appropriate sources to replace the broodstock for the Nimbus Hatchery steelhead program exist in the Upper American River, above Nimbus and Folsom dams. We show that all Upper American River O. mykiss sampled share ancestry with other populations in the Central Valley steelhead distinct population segment, with limited introgression from out-of-basin sources in some areas. Furthermore, some Upper American River populations retain adaptive genomic variation associated with a migratory life history, supporting the hypothesis that these populations display adfluvial migratory behavior. Together, these results provide insights into the evolution of trout populations above barrier dams. We conclude that some Upper American River O. mykiss populations represent genetically appropriate sources from which fisheries managers could potentially develop a new broodstock for the Nimbus Hatchery steelhead program to reestablish a native anadromous population in the Lower American River and contribute to recovery of the threatened Central Valley steelhead distinct population segment.

Genetic changes underlying adaptation vary greatly in terms of complexity and, within the same species, genetic responses to similar selective pressures may or may not be the same. We examine both complex (supergene) and simple (SNP) genetic variants occurring in populations of rainbow trout (Oncorhynchus mykiss) independently isolated from ocean access and compared them to each other and to an anadromous below-barrier population representing their ancestral source to search for signatures of both parallel and nonparallel adaptation. All landlocked populations displayed an increased frequency of a large inversion on chromosome Omy05, while 3 of the 4 populations exhibited elevated frequencies of another inversion located on chromosome Omy20. In addition, we identified numerous regions outside these 2 inversions that also show significant shifts in allele frequencies consistent with adaptive evolution. However, there was little concordance among above-barrier populations in these specific genomic regions under selection. In part, the lack of concordance appears to arise from ancestral autopolyploidy in rainbow trout that provides duplicate genomic regions of similar functional composition for selection to act upon. Thus, while selection acting on landlocked populations universally favors the resident ecotype, outside of the major chromosomal inversions, the resulting genetic changes are largely distinct among populations. Our results indicate that selection on standing genetic variation is likely the primary mode of rapid adaptation, and that both supergene complexes and individual loci contribute to adaptive evolution, further highlighting the diversity of adaptive genomic variation involved in complex phenotypic evolution.

Human-driven evolution can impact the ecological role and conservation value of impacted populations. Most evolutionary restoration approaches focus on manipulating gene flow, but an alternative approach is to manipulate the selection regime to restore historic or desired trait values. Here we examined the potential utility of this approach to restore anadromous migratory behavior in coastal California steelhead trout (Oncorhynchus mykiss) populations. We evaluated the effects of natural and anthropogenic environmental variables on the observed frequency of alleles at a genomic marker tightly associated with migratory behavior across 39 steelhead populations from across California, USA. We then modeled the potential for evolutionary restoration at sites that have been impacted by anthropogenic barriers. We found that complete barriers such as dams are associated with major reductions in the frequency of anadromy-associated alleles. The removal of dams is therefore expected to restore anadromy significantly. Interestingly, accumulations of large numbers of partial barriers (passable under at least some flow conditions) were also associated with significant reductions in migratory allele frequencies. Restoration involving the removal of partial barriers could be evaluated alongside dam removal and fishway construction as a cost-effective tool to restore anadromous fish migrations. Results encourage broader consideration of in situ evolution during the development of habitat restoration projects. This article is protected by copyright. All rights reserved.

As highlighted by many of the papers in this issue, research on the genomic basis of adaptive phenotypic variation in natural populations has made spectacular progress in the past few years, largely due to the advances in sequencing technology and analysis. Without question, the resulting genomic data will improve the understanding of regions of the genome under selection and extend knowledge of the genetic basis of adaptive evolution. What is far less clear, but has been the focus of active discussion, is how such information can or should transfer into conservation practice to complement more typical conservation applications of genetic data. Before such applications can be realized, the evolutionary importance of specific targets of selection relative to the genome-wide diversity of the species as a whole must be evaluated. The key issues for the incorporation of adaptive genomic variation in conservation and management are discussed here, using published examples of adaptive genomic variation associated with specific phenotypes in salmonids and other taxa to highlight practical considerations for incorporating such information into conservation programmes. Scenarios are described in which adaptive genomic data could be used in conservation or restoration, constraints on its utility and the importance of validating inferences drawn from new genomic data before applying them in conservation practice. Finally, it is argued that an excessive focus on preserving the adaptive variation that can be measured, while ignoring the vast unknown majority that cannot, is a modern twist on the adaptationist programme that Gould and Lewontin critiqued almost 40 years ago.

Steelhead (Oncorhynchus mykiss) populations have declined dramatically in many parts of their range in North America, most critically in Southern California, where these anadromous trout are now classified as ‘Endangered’ under the United States Endangered Species Act. The widespread introduction of hatchery rainbow trout, the domesticated freshwater resident form of the species O. mykiss, is one factor threatening the long-term persistence of native steelhead and other trout populations. To identify where native fish of coastal steelhead lineage remained, we performed a population genetic analysis of microsatellite and SNP genotypes from O. mykiss populations at the extreme southern end of their range in Southern California, USA and Baja California, Mexico. In the northern part of this region, nearly all populations appeared to be primarily descendants of native coastal steelhead. However, in the southern, more urbanized part of this region, the majority of the sampled populations were derived primarily from hatchery trout, indicating either complete replacement of native fish or a strong signal of introgression overlaying native ancestry. Nevertheless, these genetically introgressed populations represent potentially critical genetic resources for the continued persistence of viable networks of O. mykiss populations, given the limited native ancestry uncovered in this region and the importance of genetic variation in adaptation. This study elucidates the geographic distribution of native trout populations in this region, and serves as a baseline for evaluating the impacts of hatchery trout on native O. mykiss populations and the success of steelhead conservation and recovery efforts.

From 2002 to 2010, the jumbo squid (Dosidicus gigas) has been regularly encountered in large numbers throughout the California Current System (CCS). This species, usually found in subtropical waters, could affect coastal pelagic ecosystems and fisheries as both predator and prey. Neither the abundance of jumbo squid nor the optimal ocean conditions in which they flourish are well known. To understand better the potential impacts of this species on both commercial fisheries and on food-web structure we collected nearly 900 specimens from waters of the CCS, covering over 201 of latitude, over ar ange of depths and seasons. We used demographic information (size, sex, and maturity state) and analyzed stomach contents using morphological and molecular methods to best understand the foraging ecology of this species in different habitats of the CCS. Squid were found to consume a broad array of prey. Prey in offshore waters generally reflected the forage base reported in previous studies (mainly mesopelagic fishes and squids), whereas in more coastal waters (shelf, shelf break and slope habitats) squid foraged on a much broader mix that included substantial numbers of coastal pelagic fishes (Pacific herring and northern anchovy, as well as osmerids and salmonids in northern waters) and groundfish (Pacific hake, several species of rockfish and flatfish). We propose a seasonal movement pattern, based on size and maturity distributions along with qualitative patterns of presence or absence, and discuss the relevance of both the movement and distribution of jumbo squid over space and time. We find that jumbo squid are a generalist predator, which feeds primarily on small, pelagic or mesopelagic micronekton but also on larger fishes when they are available. We also conclude that interactions with and potential impacts on ecosystems likely vary over space and time, in response to both seasonal movement patterns and highly variable year-to-year abundance of the squid themselves. Published by Elsevier Ltd.

– Differential rates of anadromy between males and females are common in partially migratory salmonid populations, but this pattern is not fully clear for Oncorhynchus mykiss (rainbow trout/steelhead) from the limited but mixed data available. In particular, there are very few data on sex ratios of juvenile and nonanadromous (resident) fish to help assess sex composition of various life stages and life-history types. We used a recently developed Y-chromosome genetic marker to assess sex ratio of stream-dwelling (i.e., juvenile and nonanadromous) O. mykiss in a small coastal basin in central California, USA. We analysed 384 samples collected from three contiguous study reaches over 3 years. Sex ratio was 1:1 among juvenile-sized O. mykiss (

Freshwater-resident coastal rainbow trout Oncorhynchus mykiss irideus and the anadromous form of the subspecies, coastal steelhead (summer and winter runs), are present throughout the lower Klamath River–Trinity River system. Although coastal steelhead and other anadromous salmonids historically migrated into the Upper Klamath Basin (which encompasses the upper Klamath River and Upper Klamath Lake) and associated tributaries, the construction of Copco Dam in 1918 and Iron Gate Dam in 1962 stopped all upstream migration of fish past these barriers. In the Upper Klamath Lake basin, native Upper Klamath Lake redband trout O. mykiss newberrii are found along with coastal rainbow trout that were trapped above the dams or stocked from hatchery sources. However, relatively little is known about the genetic relationships among the O. mykiss populations within the Upper Klamath Basin. A population genetic analysis based on data from 17 variable microsatellite loci was conducted for samples collected in th...

Novel genetic resources now make it possible to directly assess the effects of natural selection on specific regions of the salmonid genome. Natural selection on specific genetic loci will also affect the variation in linked flanking regions through “hitchhiking” effects, causing greater differentiation between populations than would be expected from purely neutral processes. Here we identify candidate genomic regions for the effects of differential natural selection in two closely related populations of steelhead–rainbow trout Oncorhynchus mykiss separated for the last century following anthropogenic introduction above a barrier waterfall in a coastal California stream. A set of 110 expressed sequence tag (EST)-linked and 188 anonymous microsatellite loci, most of which are mapped, were chosen to provide distributed coverage of all linkage groups in the O. mykiss genome. A genome screen was then performed to identify genomic regions under divergent selection. Multiple complementary statistical m...

*NOAA Southwest Fisheries Science Center, National MarineFisheries Service, 110 Shaffer Road, Santa Cruz, CA 95060,USA, †Department of Ecology and Evolutionary Biology,University of California, Santa Cruz, CA, USA, ‡Department ofApplied Math and Statistics, University of California, SantaCruz, CA, USAReceived 11 March 2009; revision received 30 April 2009;accepted 5 May 2009The effective size, N

Molecular genetic analysis has long been used to identify species or populations that otherwise may be difficult to distinguish. More than 100 species of rockfish (genus Sebastes) occur worldwide, and more than 50 species may be found in relatively small regions, such as the Monterey Bay or Channel Islands in central and southern California. Many species are morphologically similar, particularly during the early larval stages, and identification to the species level is time-consuming and problematic for some groups. We describe a simple genetic method for the rapid identification of rockfish species by means of multilocus nuclear genotypes from a panel of six microsatellite loci. Application to a set of known rockfish tissue samples, including fish collected in different parts of their geographic ranges and species not represented in the reference data set, resulted in high assignment accuracy for the represented species and exclusion of the nonrepresented species. Members of the subgenus Pteropo...

We used genetic data from 7 microsatellite loci to determine the frequency of multiple paternity in clutches of giant Amazon river turtles, Podocnemis expansa, from the Orinoco River in Venezuela. Among hatchlings sampled from 32 clutches, paternity analysis found that a minimum of 10.3% could conclusively be shown to have been sired by more than one male. We contrast this result with those from another population of this species, as well as other species of turtles, and discuss the importance of documenting patterns of paternity in different populations of a given species and considering the effects of ecological differences among populations on female mating behavior.

Harbour seals sometimes breed along inland travel corridors where females become clustered in space and time and males establish underwater acoustic display territories similar to terrestrial arenas known as resource-based leks. Under these conditions, we predicted that higher levels of polygyny would be observed than has been previously reported for this species mating in open coast environments without travel corridors. Reproductive success (RS) of 70 males was measured using 20 microsatellite DNA loci and likelihood-based paternity analysis of 136 offspring collected over 3 years. Most males were assigned either zero or one paternity with 80% confidence. The greatest number of pups assigned to one male in a season was two. Variance in RS was higher for males than females (which are biologically limited to one offspring per year) indicating low to mild polygyny. In addition, distributions of relatedness values among pups within year classes did not differ significantly from a simulated distribution with R = 0, indicating that half-siblings were uncommon. Overall, polygyny levels were low relative to terrestrial pinniped mating systems and similar to observations from a harbour seal population along an open coast. Due to large confidence intervals associated with our results, we cannot rule out the hypothesis that a travel corridor might increase the degree of polygyny skew relative to that observed in open coast environments. Habitat appeared to influence male strategies as the most successful males in open coast environments patrolled offshore, while the most successful male in this study defended a territory along the travel corridor.

Giant Amazon river turtles, Podocnemis expansa, are indigenous to the Amazon, Orinoco, and Essequibo River basins, and are distributed across nearly the entire width of the South American continent. Although once common, their large size, high fecundity, and gregarious nesting, made P. expansa especially vulnerable to over-harvesting for eggs and meat. Populations have been severely reduced or extirpated in many areas throughout its range, and the species is now regulated under Appendix II of the Convention on International Trade in Endangered Species. Here, we analyse data from mitochondrial DNA sequence and multiple nuclear microsatellite markers with an array of complementary analytical methods. Results show that concordance from multiple data sets and analyses can provide a strong signal of population genetic structure that can be used to guide management. The general lack of phylogeographic structure but large differences in allele and haplotype frequencies among river basins is consistent with fragmented populations and female natal-river homing. Overall, the DNA data show that P. expansa populations lack a long history of genetic differentiation, but that each major tributary currently forms a semi-isolated reproductive population and should be managed accordingly.

Mating systems within the genus Peromyscus have traditionally been inferred from field observations of spatial relationships of males and females and from laboratory behavioral studies. The majority of species within Peromyscus are assumed to be promiscuous, but rarely have these conclusions been verified with molecular data. Genotypes constructed from 4 microsatellite loci were used to determine paternity in 10 litters of the canyon mouse (Peromyscus crinitus). We applied 3 criteria for paternity assignment: direct observation of paternal alleles, correlation of sampled male and offspring genotypes (mothers known) including spatial relationship data, and application of a likelihood estimator. Multiple paternity occurred in a minimum of 20% of the litters, yet we found no evidence that would indicate that any putative father sired 2 or more litters. Dispersal of males between the time of copulation and parturition was minimal (7.5‐70 m) in most cases, but 1 male was captured in a rock outcropping separate from that of his sired litter (174 m). Our use of 3 different criteria allowed a greater number of male paternity assignments to be inferred than would have been possible when using software program CERVUS alone, and increased confidence in these results.

Both the ability to generate DNA data and the variety of analytical methods for conservation genetics are expanding at an ever-increasing pace. Analytical approaches are now possible that were unthinkable even five years ago due to limitations in computational power or the availability of DNA data, and this has vastly expanded the accuracy and types of information that may be gained from population genetic data. Here we provide a guide to recently developed methods for population genetic analysis, including identification of population structure, quantification of gene flow, and inference of demographic history. We cover both allele-frequency and sequence-based approaches, with a special focus on methods relevant to conservation genetic applications. Although classical population genetic approaches such as Fst (and its derivatives) have carried the field thus far, newer, more powerful, methods can infer much more from the data, rely on fewer assumptions, and are appropriate for conservation genetic management when precise estimates are needed.

When females receive no direct benefits from multiple matings, concurrent multiple paternity is often explained by indirect genetic benefits to offspring. To examine such possibilities, we analyzed genetic paternity for 1,272 hatchlings, representing 227 clutches, from a nesting population of painted turtles (Chrysemys picta) on the Mississippi River. Goals were to quantify the incidence and distribution of concurrent multiple paternity across clutches, examine temporal patterns of sperm storage by females, and deduce the extent to which indirect benefits result from polyandrous female behaviors. Blood samples from adult males also allowed us to genetically identify the sires of surveyed clutches and to assess phenotypic variation associated with male fitness. From the genetic data, female and male reproductive success were deduced and then interpreted together with field data to evaluate possible effects of female mating behaviors and sire identity on offspring fitness. We document that more than 30% of the clutches were likely fathered by multiple males, and that presence of multiple paternity was positively correlated with clutch size. Furthermore, the data indicate that the second male to mate typically had high paternity precedence over the first.

Molecular polymorphisms have been used in a variety of ways to estimate both effective and local census population sizes in nature. A related approach for estimating the current size of a breeding population, explored here for the first time, is the use of genetic 'marks' reconstructed for otherwise unknown parents in paternity or maternity analyses of progeny arrays. This method provides interesting similarities and contrasts to traditional mark-recapture methods based on physical tags. To illustrate, this genetic method is applied to a population of painted turtles on the Mississippi River to estimate the number of successfully breeding males. Non-genetic mark-recapture approaches were also applied to animals trapped at this location. Results demonstrate that such genetic data on parentage can be helpful not only in estimating contemporary population sizes, but also in providing additional information, not present in customary mark-recapture data, about possible extended movements of breeding individuals and the size of the pool of mates which they encounter.

Most studies of genetic parentage in natural populations have been limited to a single breeding season or reproductive episode and, thus, provide only a snapshot of individuals' mating behaviours. Female turtles can store viable sperm in their reproductive tracts for as long as several years, but the extent to which this capacity is utilized in nature has remained unknown. Here, we employ microsatellite markers to assess genetic paternity in successive clutches of individually marked, free-ranging female painted turtles (Chrysemys picta) over a four year period. The genetic data from 113 clutches from this natural population demonstrate that most females (80.5%) remated each year and that each female generally used a single male's sperm to fertilize all clutches laid within a year. However, sperm usage among females varied considerably, and some females apparently used sperm that had been stored for up to three years to fertilize some or all eggs laid in consecutive nesting seasons. Thus, remating by females is not necessary for continued offspring production from a given sire. Furthermore, 13.2% of all clutches examined showed evidence of multiple paternity, and the genetic paternity patterns across years suggest a 'last in, first out' operation of the females' sperm storage tubules.

As evidenced by the articles in this volume, a recent increase in interest in the mating systems of poikilothermic vertebrates has focused primarily on fishes, a few amphibians, and squamate reptiles. Turtles by contrast have received relatively little attention, yet they display a wide variety of mating behaviors and life-history characteristics that make them excellent candidates for addressing several aspects of genetic parentage that should contribute to a broader understanding of animal reproductive strategies. Here we focus on genetic studies of the mating systems and reproductive patterns of turtles, specifically with respect to multiple paternity and long-term sperm storage. These phenomena highlight the importance of a temporally extended perspective on patterns of individual reproductive success.

The phylogenetic relationships among populations of the fossorial California legless lizard, Anniella pulchra, were examined by sequencing a 990-bp region of the mitochondrial cytochrome b gene. The mitochondrial DNA gene tree was then compared with the geographic distributions of two currently recognized subspecies: A. p. nigra, a melanic form restricted to two disjunct coastal populations, and A. p. pulchra, a more widely distributed, silvery form. We tested the null hypothesis that all A. p. nigra form a clade that is monophyletic with respect to A. p. pulchra. Our results strongly reject the monophyletic origin of the melanic forms and suggest that the two populations of the nominal subspecies A. p. nigra may have arisen independently from different ancestral populations in a parallel evolutionary response to selection in cool, coastal habitats.