Implications of Large-Effect Loci for Conservation: A Review and Case Study with Pacific Salmon.

The increasing feasibility of assembling large genomic datasets for non-model species presents both opportunities and challenges for applied conservation and management. A popular theme in recent studies is the search for large-effect loci that explain substantial portions of phenotypic variance for a key trait(s). If such loci can be linked to adaptations, 2 important questions arise: 1) Should information from these loci be used to reconfigure conservation units (CUs), even if this conflicts with overall patterns of genetic differentiation? 2) How should this information be used in viability assessments of populations and larger CUs? In this review, we address these questions in the context of recent studies of Chinook salmon and steelhead (anadromous form of rainbow trout) that show strong associations between adult migration timing and specific alleles in one small genomic region. Based on the polygenic paradigm (most traits are controlled by many genes of small effect) and genetic data available at the time showing that early-migrating populations are most closely related to nearby late-migrating populations, adult migration differences in Pacific salmon and steelhead were considered to reflect diversity within CUs rather than separate CUs. Recent data, however, suggest that specific alleles are required for early migration, and that these alleles are lost in populations where conditions do not support early-migrating phenotypes. Contrasting determinations under the US Endangered Species Act and the State of California's equivalent legislation illustrate the complexities of incorporating genomics data into CU configuration decisions. Regardless how CUs are defined, viability assessments should consider that 1) early-migrating phenotypes experience disproportionate risks across large geographic areas, so it becomes important to identify early-migrating populations that can serve as reliable sources for these valuable genetic resources; and 2) genetic architecture, especially the existence of large-effect loci, can affect evolutionary potential and adaptability.

Genomewide association analyses of fitness traits in captive-reared Chinook salmon: Applications in evaluating conservation strategies.

A novel application of genomewide association analyses is to use trait-associated loci to monitor the effects of conservation strategies on potentially adaptive genetic variation. Comparisons of fitness between captive- and wild-origin individuals, for example, do not reveal how captive rearing affects genetic variation underlying fitness traits or which traits are most susceptible to domestication selection. Here, we used data collected across four generations to identify loci associated with six traits in adult Chinook salmon (Oncorhynchus tshawytscha) and then determined how two alternative management approaches for captive rearing affected variation at these loci. Loci associated with date of return to freshwater spawning grounds (return timing), length and weight at return, age at maturity, spawn timing, and daily growth coefficient were identified using 9108 restriction site-associated markers and random forest, an approach suitable for polygenic traits. Mapping of trait-associated loci, gene annotations, and integration of results across multiple studies revealed candidate regions involved in several fitness-related traits. Genotypes at trait-associated loci were then compared between two hatchery populations that were derived from the same source but are now managed as separate lines, one integrated with and one segregated from the wild population. While no broad-scale change was detected across four generations, there were numerous regions where trait-associated loci overlapped with signatures of adaptive divergence previously identified in the two lines. Many regions, primarily with loci linked to return and spawn timing, were either unique to or more divergent in the segregated line, suggesting that these traits may be responding to domestication selection. This study is one of the first to utilize genomic approaches to demonstrate the effectiveness of a conservation strategy, managed gene flow, on trait-associated-and potentially adaptive-loci. The results will promote the development of trait-specific tools to better monitor genetic change in captive and wild populations.

Effectiveness of managed gene flow in reducing genetic divergence associated with captive breeding.

Captive breeding has the potential to rebuild depressed populations. However, associated genetic changes may decrease restoration success and negatively affect the adaptive potential of the entire population. Thus, approaches that minimize genetic risks should be tested in a comparative framework over multiple generations. Genetic diversity in two captive-reared lines of a species of conservation interest, Chinook salmon (Oncorhynchus tshawytscha), was surveyed across three generations using genome-wide approaches. Genetic divergence from the source population was minimal in an integrated line, which implemented managed gene flow by using only naturally-born adults as captive broodstock, but significant in a segregated line, which bred only captive-origin individuals. Estimates of effective number of breeders revealed that the rapid divergence observed in the latter was largely attributable to genetic drift. Three independent tests for signatures of adaptive divergence also identified temporal change within the segregated line, possibly indicating domestication selection. The results empirically demonstrate that using managed gene flow for propagating a captive-reared population reduces genetic divergence over the short term compared to one that relies solely on captive-origin parents. These findings complement existing studies of captive breeding, which typically focus on a single management strategy and examine the fitness of one or two generations.

MORPHOLOGICAL DIVERSIFICATION AND ADAPTIVE RADIATION: A COMPARISON OF TWO DIVERSE LIZARD CLADES.

We compared the morphological diversity (i.e., the amount of morphological space occupied) of two similar clades, the lizard genera Anolis and Sceloporus. These species-rich monophyletic clades are similar in body size, age of origin, and many aspects of their natural history. We examined a number of morphological traits whose variation is likely to represent adaptation to different aspects of the environment, including body size, limb proportions, head dimensions, and tail length. Examination of the position of species in multidimensional space, based on a principal components analysis, indicates that the morphological diversity of Anolis, which we refer to as disparity, is significantly greater than that of Sceloporus. One potential explanation for this pattern is that morphological diversification in Anolis was facilitated by the evolution of subdigital toe-pads, which allow anoles to use the environment in ways not available to Sceloporus. The geographic location of diversification (tropical and subtropical for Anolis, arid for Sceloporus) may also have been important.