Evidence for the genetic basis and epistatic interactions underlying ocean‐ and river‐maturing ecotypes of Pacific Lamprey (Entosphenus tridentatus) returning to the Klamath River, California

Abstract

Surveys of genomic variation have improved our understanding of the relationship between fitness‐related phenotypes and their underlying genetic basis. In some cases, single large‐effect genes have been found to underlie important traits; however, complex traits are expected to be under polygenic control and elucidation of multiple gene interactions may be required to fully understand the genetic basis of the trait. In this study, we investigated the genetic basis of the ocean‐ and river‐maturing ecotypes in anadromous Pacific lamprey (Entosphenus tridentatus). In Pacific lamprey, the ocean‐maturing ecotype is distinguished by advanced maturity of females (e.g., large egg mass) at the onset of freshwater migration relative to immature females of the river‐maturing ecotype. We examined a total of 219 adult Pacific lamprey that were collected at‐entry to the Klamath River over a 12‐month period. Each individual was genotyped at 308 SNPs representing known neutral and adaptive loci and measured at morphological traits, including egg mass as an indicator of ocean‐ and river‐maturing ecotype for females. The two ecotypes did not exhibit genetic structure at 148 neutral loci, indicating that ecotypic diversity exists within a single population. In contrast, we identified the genetic basis of maturation ecotypes in Pacific lamprey as polygenic, involving two unlinked gene regions that have a complex epistatic relationship. Importantly, these gene regions appear to show stronger effects when considered in gene interaction models than if just considered additive, illustrating the importance of considering epistatic effects and gene networks when researching the genetic basis of complex traits in Pacific lamprey and other species.

Genomic islands of divergence infer a phenotypic landscape in Pacific lamprey

“…The chromosome that showed the highest association with body size was chromosome 02 and these associations were greatest in the data sets from furthest upstream locations (T_BON, S_BON, and JDD). This chromosome 02 association with body size was consistent among data sets located both within and outside the Columbia River basin (Parker et al., 2019).…”

“…Although the average body sizes differed across sites and sexes (WFA♀ were larger on average than WFA♂), the trends were consistent between data sets (Figure 3a). Further, similar genotype and average length associations have been detected in Pacific lamprey collected from the Klamath River (634, 602, and 557 mm for the AA, AC, and CC genotypes at Etr_5317, respectively; Parker et al., 2019).…”

“…Several traits in Pacific lamprey have been found to have a genetic basis. These include body size, reproductive migration‐timing (Hess et al., 2014, 2015), and advanced maturity of females at onset of freshwater migration (i.e., ocean‐maturing versus river‐maturing ecotypes, Parker, Hess, Narum, & Kinziger, 2019). There also appears to be evidence for statistical linkage of multiple loci that show high divergence in the species’ range (Hess, Campbell, Close, Docker, & Narum, 2013).…”

RapidRat: Development, validation and application of a genotyping-by-sequencing panel for rapid biosecurity and invasive species management

“…Moving forward, GT-seq and other targeted amplicon sequencing approaches hold great promise for informing conservation and management of biodiversity [66]. Originally demonstrated in steelhead trout [24], GT-seq has been subsequently applied to the study of other fish species, including redband trout [66], brook trout [67], Pacific lamprey [68], and walleye [69]. More recently, the efficacy of using GT-seq for genotyping minimally-invasive samples has been demonstrated [46], and successfully applied to further understanding of the molecular ecology and conservation status of the at-risk Western rattlesnake [70].…”

Natural Recolonization by Pacific Lampreys in a Southern California Coastal Drainage: Implications for Their Biology and Conservation

“…; Parker et al. ). Redd construction was photodocumented in Stenner Creek in 2019 just above where ammocoetes were encountered in this study (Doug Platt, Melia Green, California Conservation Corps, and Freddy Otte, City of San Luis Obispo, personal communication).…”