- One such example occurred when sea lamprey ( Petromyzon marinus. - heterozygosity and π ) for sea lamprey collected from native (Connecticut River), native but recently colonized (Lake Champlain), and invasive (Lake Michigan) populations, assessed genetic. - Champlain populations, respectively, compared to individuals from the Connecticut River, suggesting that sea lamprey populations underwent a genetic bottleneck during colonization. - identification of outlier genes underlying key life history traits known to have changed in invasive sea lamprey populations (e.g. - Keywords: Founder effects, Genetic bottleneck, Invasive species, Selection, Rapid genetic adaptation, RNA-seq, Sea lamprey Petromyzon marinus. - One such example occurred when sea lamprey (Petromyzon marinus), a parasitic, jawless vertebrate native to the northern Atlantic, invaded the Laurentian Great Lakes.. - During their larval stages, sea lamprey burrow into soft and sandy substrates in freshwater streams and filter feed for an average of four to eight years (reported range is 2–19 years) [8]. - After undergoing a series of be- havioral and physiological modifications essential for a hematophagous, parasitic lifestyle, larval sea lamprey (i.e., ammocoetes) transform into parasitic juveniles [9]. - Once in the ocean, sea lamprey parasitize many host species such as herring (Clupea harengus), mackerel (Scomber scombrus), and Atlantic salmon (Salmo salar) [10]. - Juvenile sea lamprey attach to their hosts using sharp teeth and are able to continuously feed on the blood and tissue of their hosts by secreting anticoagulants [11]. - The parasitic feeding stage in sea lamprey lasts between 20 to 36 months, after which sea lamprey return to rivers and streams for. - Instead of returning to their natal streams, like many other anadromous fishes (e.g., salmon), sea lamprey rely on a pheromone produced by larvae in streams and rivers as a cue for migration [12–15]. - Thus, the choice of which stream to spawn in is largely driven by larval abundance, where high larval abundance results in more pheromone released and can generate a strong signal to attract adult sea lamprey for spawning. - Sea lamprey are native to the northern Atlantic coast [17], and migrated into Lake Ontario and Lake Champlain, where they were first observed in 1835 and 1841, respectively [18–. - The construction and improvement of shipping canals in the early 1800s allowed sea lamprey to expand their ranges to Lake Erie and then colonize Lakes Huron, Michigan, and Superior . - The first documented observations of sea lamprey for Lake Erie was in Lake Michigan in Lake Huron in and Lake Superior in 1946 [20]. - The ecology and environmental conditions found in the Great Lakes are substantially different from those found throughout the sea lamprey’s native range [17], and have changed some of sea lamprey’s life history characteristics. - For example, invasive sea lamprey spend their parasitic life history stage entirely in the freshwater environment of the Great Lakes instead of migrating to the ocean. - Thus, invasive sea lamprey never acclimate to high-salinity ocean environments. - Sea lamprey in the Great Lakes also exhibit a faster growth rate, a shorter larval stage, a smaller adult body size, and a lower. - Lastly, invasive sea lamprey spend more time feeding parasitically on a single host individ- ual, and greater numbers of individual sea lamprey are often found attached to a single adult fish in the Great Lakes than in the Atlantic Ocean.. - While these differences in life history characteristics of invasive sea lamprey are suggestive of genetic adaptation, many of these traits may simply be a plastic response to different environments [27–29]. - Determining which genes have responded to selection in the novel, recently colo- nized environment is valuable for understanding rapid genetic adaptation (i.e., occurring in fewer than 200 years in invasive sea lamprey) to new environments in both sea lamprey and other species. - To achieve this objective, we sampled larval sea lamprey from three locations: (1) the Connecticut River, a native-range tributary of the Atlantic Ocean, (2) Lake Michigan, where sea lamprey are invasive, and (3) Lake Champlain, an additional freshwater environ- ment that sea lamprey colonized through natural migra- tions (Fig. - Although sea lamprey may be native to Lake Champlain [7], they still needed to adjust to a novel, entirely-freshwater environment with vastly different eco- logical conditions. - By conducting this set of analyses, we aim to answer two primary questions: (1) Did sea lamprey populations colonizing Lake Michigan and Lake Champlain undergo a genetic bottleneck during colonization (i.e., founder effects), and (2) what genes have responded to selection in the novel environments and how do they relate to the documented phenotypic shifts in life history traits?. - Population structure and observed heterozygosity We collected 565 larval sea lamprey from the Manistee River in Lake Michigan, 517 larval sea lamprey from Corbeau Creek and the LaPlatte River in Lake Cham- plain, and 404 larval sea lamprey from the Connecticut River in 2016 (Fig. - Using the model-based clustering methods imple- mented in STRUCTURE (version all sea lamprey were assigned to their collection locations (population membership coefficients ranged from 0.961 to 1 for Lake Michigan population, 0.954 to 1 for Lake Champlain population, and 0.969 to 1 for Connecticut River population) with K set to 3 (Fig. - If we as- sumed all 41 samples originated from two populations (i.e., K = 2), sea lamprey collected from Lake Michigan and Connecticut River clustered as one population while those from Lake Champlain were assigned to the other (Fig. - Larval sea lamprey were collected from Lake Michigan, Lake Champlain, and the Connecticut River, where the numbers reflect the number of muscle and liver samples of larval sea lamprey that were sequenced and used in this study (a). - Larval sea lamprey collected from the three locations cluster clearly into three distinct groups (b). - Sea lamprey have 99 chromosomes, among which the first 90 are assembled. - S7), only appear when comparing Lake Michigan and Connecticut River sea lamprey, suggesting that Lake Michigan sea lamprey may have adapted to their novel, in- troduced range by adjusting their growth (Fig. - This difference may reflect different evolu- tionary strategies the two recently colonized sea lamprey populations adopt to adapt to their novel environments, one of which is mediated exclusively at the transcriptomic level while the other is mediated through both DNA tran- scription and translation.. - Six out of 121 outlier genes in comparison between Lake Michigan and Connecticut River (i.e., GHR, PGR, TTC25, STARD10, OXCT1, SLC25A15) and two out of 43 outlier genes in comparison between Lake Champlain and Connecticut River (i.e., DIN4, PYGL) may poten- tially explain changes in growth, reproduction, and bio- energetics in sea lamprey in response to novel ecological conditions (Fig. - It has been shown that the urea ex- cretion rate of sea lamprey removed from sharks is ~ 5 to 30 times higher than that of those removed from rain- bow trout [48], suggesting that urea excretion in sea. - Thus, adaptive differentiation at SLC25A15 may be a re- flection of changes in sea lamprey’s prey and their capacity of adjusting nitrogen metabolism depending on which host fishes are available. - This striking result suggests that sea lamprey in Lake Michigan and Lake Champlain may have experienced parallel evolution whereby the differences in ecological conditions between the two lakes may not be large enough to exert strong differential selection when adapt- ing to the novel environment. - Connecticut River: mean F ST = 0.123) and sea lamprey collected from Lake Michigan, Lake Champlain and Connecticut River clearly clustered into three distinct groups (Fig. - only a small num- ber of sea lamprey may have been able to successfully colonize these environments [49].. - Candidate genes underlying rapid genetic adaptation Invasive sea lamprey in the Great Lakes exhibit a faster growth rate, a shorter larval stage, a smaller adult body size, and a lower fecundity [25, 26]. - Sea lamprey have very large effective population sizes, so we suggest that, at genes related to these changes, selection is most likely to have acted on the standing genetic variation already present within the population and did not depend on de novo mutations. - As such, GHR plays a crucial role in fish growth [36] and may account for the faster growth rate and smaller adult size of sea lamprey colonizing the Great Lakes and Lake Champlain. - Additionally, selection at the outlier genes, PGR, STARD10, and TTC25, could explain the lower fecundity observed in Lake Michigan sea lamprey since these genes are known to affect ovula- tion and sperm production and quality [37, 38]. - growth, reproduction, bioenergetics) in sea lamprey from Lake Michigan, Lake Champlain, and Connecticut River are shown along corresponding chromosomes with SNPs located on introns, untranslated regions (UTR), and coding regions (CDS) indicated with different colors (left panels). - This re- sult may suggest that changes in life history strategies essential for sea lamprey’s colonization in Lake Cham- plain may be mediated by plasticity or the genetic differ- entiation between these two populations driving changes in life history strategies is not strong enough to be detected.. - In the Great Lakes, sea lamprey spend more time feed- ing on a single host, and more sea lamprey are found to attach to one adult fish than in the Atlantic Ocean [25, 26]. - This observation could be driven by the high ratio of sea lamprey to host fishes, suggesting that food sources may have been limited in the invasive range given the high abundance of sea lamprey prior to treat- ment with lampricides. - While OXCT1 is identified in the comparison between Lake Michigan and Connecticut River, PYGL and DIN4 are detected in the comparison between Lake Champlain and Connecticut River, suggesting that sea lamprey in both Lake Michigan and Lake Champlain have responded to the selection imposed by the differ- ences in food sources and availability in these novel, freshwater environments.. - Instead of migrating to the ocean, Lake Michigan and Lake Champlain sea lamprey spend their entire life in freshwater and never acclimate to salt water environ- ments. - Previous work has shown that 11-deoxycortisol, Na-K-Cl cotransporter 1, and Na + -K + -ATPase may en- gage in sea lamprey’s osmoregulation [53–55]. - related to sea lamprey’s adaptation to freshwater envi- ronments could be due to a lack of power (e.g., sample sizes). - Alternatively, sea lamprey may respond to changes in salinity plastically by differentially expressing relevant genes at the transcriptomic level, and the selec- tion imposed by differences in salinity may not be strong enough to shift allele frequencies among populations at the genomic level [54, 59].. - While we have identified a series of outlier genes that may be driving sea lamprey’s rapid adaption to novel environ- ments, several outstanding questions remain. - Although our study identified outlier genes that are likely driving rapid adaptation at the genomic level, we do not know yet how these genes perform at the proteomic and metabolic level to support variation at the physiological, individual, and population level in recently colonized sea lamprey populations. - How these genes work concurrently and coordin- ate to help sea lamprey colonize new environments remains unknown and merits further investigation. - Determining whether these changes in life his- tory associated genes we documented here are driven by the natural environment, treatment with TFM, or both will be important for the successful management of inva- sive sea lamprey.. - Utilizing genome-wide SNPs called from RNA-seq data, we found that two sea lamprey populations lost genome- wide genetic diversity when colonizing novel, entirely freshwater environments. - Evidence of a response to se- lection at eight outlier genes suggest that sea lamprey rapidly adapted to their novel, freshwater environments with changes in growth, reproduction, and bioenergetics.. - Overall, our study enhances our understanding of the genes underlying sea lamprey’s life history traits, which may aid with invasive species control in the Great Lakes, and also demonstrates how introduced species can be a useful study system for shedding light on rapid genetic adaptation.. - We collected 565 larval sea lamprey from the Manistee River in Lake Michigan, 517 larval sea lamprey from Corbeau Creek and the LaPlatte River in Lake Cham- plain, and 404 larval sea lamprey from the Connecticut River in 2016 (Fig. - from each population were used to test the sensitivity of sea lamprey to TFM (see [30] for details). - These individuals were previously used to determine whether invasive sea lamprey are evolving resistance to the pesti- cide TFM (see [30] for details).. - We started by mapping RNA-seq reads to the sea lamprey genome [70] following the STAR 2-pass alignment steps. - Sea lamprey have 99 chromosomes [70], 90 of which are assembled, so we next calculated observed heterozygosity of each of the 90 assembled chromo- somes for each population by averaging observed hetero- zygosity across all loci within each chromosome in a population. - After identifying outlier SNPs, we identified cor- responding genes (i.e., outlier genes) on which outlier loci were located by mapping outlier loci to the sea lamprey genome [70] and calculated the allele fre- quency at each outlier locus. - By examining the position of outlier loci on the anno- tated sea lamprey genome [70], we determined whether an outlier SNP was located on introns, coding regions (CDS), or untranslated regions (3 ′ or 5 ′ UTR). - Population structure of Lake Michigan, Lake Champlain, and Connecticut River sea lamprey ( K . - sea lamprey have 99 chromosomes, 90 of which are assembled) and at SNPs (by SNP) calculated using 346,280 SNPs across the genome that are in Hardy- Weinberg equilibrium and in common to Lake Michigan (LM), Lake Champlain (LC) and Connecticut River (CT) populations differs signifi- cantly between each pairwise comparison (LM vs. - Sea lamprey have 99 chromosomes, 90 of which are assembled. - Z( F ST ) of all SNPs on outlier genes identified with muscle samples that may contribute to adaptation to local environments (i.e., reproduction, bioenergetics) in sea lamprey are shown along corresponding chromosomes with SNPs on introns, untranslated regions (UTR), and coding regions (CDS) indicated in different colors (left panels). - Code and scripts are available at https://github.com/ChristieLab/sea_lamprey_. - The Purdue Animal Care and Use Committee (PACUC) was informed of this study, but did not require animal care protocols for the larval sea lamprey used in this study.. - https://doi.org/10.1016/S . - Patterns of invasion and colonization of the sea lamprey ( Petromyzon marinus ) in North America as revealed by microsatellite genotypes. - Direct behavioral evidence that unique bile acids released by larval sea lamprey ( Petromyzon marinus ) function as a migratory pheromone. - The chemical ecology and potential application of the sea lamprey migratory pheromone. - https://doi.org/10.1016/S X.. - https://doi.org/10.1111/j x.. - Sea lamprey Petromyzon marinus : an exception to the rule of homing in anadromous fishes. - https://doi.org/10.1139/. - An early record of the sea lamprey ( Petromyzon marinus ) from Lake Ontario, vol. - Life history of the sea lamprey of Cayuga Lake. - Natural history of the sea lamprey ( Petromyzon marinus ) in Michigan.. - https://spo.nmfs.noaa.gov/content/natural- history-sea-lamprey-petromyzon-marinus-michigan. - Sea lamprey ( Petromyzon marinus ) in lakes Huron, Michigan, and superior: history of invasion and control, 1936 – 78. - A case history of sea lamprey control in Lake Michigan: 1979 to 1999. - Sea lamprey control in lake Champlain. - Changes in biological characteristics of the sea lamprey ( Petromyzon marinus ) as related to lamprey abundance, prey abundance, and sea lamprey control. - Occurrence, relative abundance, and size of landlocked sea lamprey ( Petromyzon marinus ) ammocoetes in relation to stream characteristics in the Great Lakes. - https://doi.org . - https://doi.org/10.1016/B . - https://doi.org/10.1016/j.. - Osmoregulatory role of the intestine in the sea lamprey ( Petromyzon marinus. - K+-2Cl − cotransporter in the gill of sea lamprey ( Petromyzon marinus. - 11-Deoxycortisol controls hydromineral balance in the most basal osmoregulating vertebrate, sea lamprey ( Petromyzon marinus. - Divergent genes encoding the putative receptors for growth hormone and prolactin in sea lamprey display distinct patterns of expression. - https://doi.org/10.1038/s . - Life history evolution of sea lamprey predicted to reduce the effectiveness of pesticide control. - The sea lamprey germline genome provides insights into programmed genome rearrangement and vertebrate evolution
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