scholarly journals Rapid genetic adaptation to recently colonized environments is driven by genes underlying life history traits

BMC Genomics ◽  
2021 ◽  
Vol 22 (1) ◽  
Author(s):  
Xiaoshen Yin ◽  
Alexander S. Martinez ◽  
Maria S. Sepúlveda ◽  
Mark R. Christie

Abstract Background Uncovering the mechanisms underlying rapid genetic adaptation can provide insight into adaptive evolution and shed light on conservation, invasive species control, and natural resource management. However, it can be difficult to experimentally explore rapid adaptation due to the challenges associated with propagating and maintaining species in captive environments for long periods of time. By contrast, many introduced species have experienced strong selection when colonizing environments that differ substantially from their native range and thus provide a “natural experiment” for studying rapid genetic adaptation. One such example occurred when sea lamprey (Petromyzon marinus), native to the northern Atlantic, naturally migrated into Lake Champlain and expanded their range into the Great Lakes via man-made shipping canals. Results Utilizing 368,886 genome-wide single nucleotide polymorphisms (SNPs), we calculated genome-wide levels of genetic diversity (i.e., heterozygosity and π) for sea lamprey collected from native (Connecticut River), native but recently colonized (Lake Champlain), and invasive (Lake Michigan) populations, assessed genetic differentiation between all populations, and identified candidate genes that responded to selection imposed by the novel environments. We observed a 14 and 24% reduction in genetic diversity in Lake Michigan and Lake Champlain populations, respectively, compared to individuals from the Connecticut River, suggesting that sea lamprey populations underwent a genetic bottleneck during colonization. Additionally, we identified 121 and 43 outlier genes in comparisons between Lake Michigan and Connecticut River and between Lake Champlain and Connecticut River, respectively. Six outlier genes that contained synonymous SNPs in their coding regions and two genes that contained nonsynonymous SNPs may underlie the rapid evolution of growth (i.e., GHR), reproduction (i.e., PGR, TTC25, STARD10), and bioenergetics (i.e., OXCT1, PYGL, DIN4, SLC25A15). Conclusions By identifying the genomic basis of rapid adaptation to novel environments, we demonstrate that populations of invasive species can be a useful study system for understanding adaptive evolution. Furthermore, the reduction in genome-wide levels of genetic diversity associated with colonization coupled with the identification of outlier genes underlying key life history traits known to have changed in invasive sea lamprey populations (e.g., growth, reproduction) illustrate the utility in applying genomic approaches for the successful management of introduced species.

2019 ◽  
Author(s):  
Daniel Selechnik ◽  
Mark F. Richardson ◽  
Richard Shine ◽  
Jayna DeVore ◽  
Simon Ducatez ◽  
...  

AbstractInvasive species often exhibit rapid evolution in their introduced ranges despite the genetic bottlenecks that are thought to accompany the translocation of small numbers of founders; however, some invasions may not fit this “genetic paradox.” The invasive cane toad (Rhinella marina) displays high phenotypic variation across its environmentally heterogeneous introduced Australian range. Here, we used three genome-wide datasets to characterize population structure and genetic diversity in invasive toads: RNA-Seq data generated from spleens sampled from the toads’ native range in French Guiana, the introduced population in Hawai’i that was the source of Australian founders, and Australia; RNA-Seq data generated from brains sampled more extensively in Hawai’i and Australia; and previously published RADSeq data from transects across Australia. We found that toads form three genetic clusters: (1) native range toads, (2) toads from the source population in Hawai’i and long-established areas near introduction sites in Australia, and (3) toads from more recently established northern Australian sites. In addition to strong divergence between native and invasive populations, we find evidence for a reduction in genetic diversity after introduction. However, we do not see this reduction in loci putatively under selection, suggesting that genetic diversity may have been maintained at ecologically relevant traits, or that mutation rates were high enough to maintain adaptive potential. Nonetheless, cane toads encounter novel environmental challenges in Australia and appear to respond to selection across environmental breaks; the transition between genetic clusters occurs at a point along the invasion transect where temperature rises and rainfall decreases. We identify loci known to be involved in resistance to heat and dehydration that show evidence of selection in Australian toads. Despite well-known predictions regarding genetic drift and spatial sorting during invasion, this study highlights that natural selection occurs rapidly and plays a vital role in shaping the structure of invasive populations.Author SummaryDespite longstanding evidence for the link between genetic diversity and population viability, the “genetic paradox” concept reflects the observation that invasive populations are successful in novel environments despite a putative reduction in genetic diversity. However, some recent studies have suggested that successful invasions may often occur due to an absence of obstacles such as genetic diversity loss or novel adaptive challenges. The recent emergence of genome-wide technologies provides us with the tools to study this question comprehensively by assessing both overall genetic diversity, and diversity of loci that underlie ecologically relevant traits. The invasive cane toad is a useful model because there is abundant phenotypic evidence of rapid adaptation during invasion. Our results suggest strong genetic divergence between native and invasive populations, and a reduction in overall genetic diversity; however, we do not see this reduction when solely assessing ecologically relevant loci. This could be for reasons that support or refute the genetic paradox. Further studies may provide perspectives from other systems, allowing us to explore how variables such as propagule size affect the fit of an invasion to the model of the paradox. Studying invasive species remains important due to their largely negative impacts on the environment and economy.


Genetics ◽  
2020 ◽  
Vol 215 (3) ◽  
pp. 813-829
Author(s):  
Matthew M. Osmond ◽  
Graham Coop

One of the most useful models in population genetics is that of a selective sweep and the consequent hitch-hiking of linked neutral alleles. While variations on this model typically assume constant population size, many instances of strong selection and rapid adaptation in nature may co-occur with complex demography. Here, we extend the hitch-hiking model to evolutionary rescue, where adaptation and demography not only co-occur but are intimately entwined. Our results show how this feedback between demography and evolution determines—and restricts—the genetic signatures of evolutionary rescue, and how these differ from the signatures of sweeps in populations of constant size. In particular, we find rescue to harden sweeps from standing variance or new mutation (but not from migration), reduce genetic diversity both at the selected site and genome-wide, and increase the range of observed Tajima’s D values. For a given initial rate of population decline, the feedback between demography and evolution makes all of these differences more dramatic under weaker selection, where bottlenecks are prolonged. Nevertheless, it is likely difficult to infer the co-incident timing of the sweep and bottleneck from these simple signatures, never mind a feedback between them. Temporal samples spanning contemporary rescue events may offer one way forward.


2018 ◽  
Vol 27 (20) ◽  
pp. 4041-4051 ◽  
Author(s):  
Janna R. Willoughby ◽  
Avril M. Harder ◽  
Jacob A. Tennessen ◽  
Kim T. Scribner ◽  
Mark R. Christie

2019 ◽  
Author(s):  
Matthew M. Osmond ◽  
Graham Coop

AbstractOne of the most useful models in population genetics is that of a selective sweep and the consequent hitch-hiking of linked neutral alleles. While variations on this model typically assume constant population size, many instances of strong selection and rapid adaptation in nature may co-occur with complex demography. Here we extend the hitch-hiking model to evolutionary rescue, where adaptation and demography not only co-occur but are intimately entwined. Our results show how this feedback between demography and evolution determines – and restricts – the genetic signatures of evolutionary rescue, and how these differ from the signatures of sweeps in populations of constant size. In particular, we find rescue to harden sweeps from standing variance or new mutation (but not from migration), reduce genetic diversity both at the selected site and genome-wide, and increase the range of observed Tajima’s D values. For a given initial rate of population decline, the feedback between demography and evolution makes all of these differences more dramatic under weaker selection, where bottlenecks are prolonged. Nevertheless, it is likely difficult to infer the co-incident timing of the sweep and bottleneck from these simple signatures, never-mind a feedback between them. Temporal samples spanning contemporary rescue events may offer one way forward.


2018 ◽  
Author(s):  
Jiarui Li ◽  
Xinyue Cheng ◽  
Runmao Lin ◽  
Shijun Xiao ◽  
Xinxin Yi ◽  
...  

AbstractGenetic adaptation to new environments is essential for invasive species. To explore the genetic underpinnings of invasiveness of a dangerous invasive species, the pinewood nematode (PWN) Bursaphelenchus xylophilus, we analysed the genome-wide variations of a large cohort of 55 strains isolated from both the native and introduced regions. Comparative analysis showed abundant genetic diversity existing in the nematode, especially in the native populations. Phylogenetic relationships and principal component analysis indicate a dominant invasive population/group (DIG) existing in China and expansion beyond, with few genomic variations. Putative origin and migration paths at a global scale were traced by targeted analysis of rDNA sequences. A progressive loss of genetic diversity was observed along spread routes. We focused on variations with a low frequency allele (<50%) in the native USA population but fixation in DIG, and a total of 25,992 single nuclear polymorphisms (SNPs) were screened out. We found that a clear majority of these fixation alleles originated from standing variation. Functional annotation of these SNP-harboured genes showed that adaptation-related genes are abundant, such as genes that encode for chemoreceptors, proteases, detoxification enzymes, and proteins involved in signal transduction and in response to stresses and stimuli. Some genes under positive selection were predicted. Our results suggest that adaptability to new environments plays essentially roles in PWN invasiveness. Genetic drift, mutation and strong selection drive the nematode to rapidly evolve in adaptation to new environments, which including local pine hosts, vector beetles, commensal microflora and other new environmental factors, during invasion process.


Viruses ◽  
2021 ◽  
Vol 13 (2) ◽  
pp. 285
Author(s):  
Cynthia R. Adams ◽  
Vicki S. Blazer ◽  
Jim Sherry ◽  
Robert Scott Cornman ◽  
Luke R. Iwanowicz

Hepatitis B viruses belong to a family of circular, double-stranded DNA viruses that infect a range of organisms, with host responses that vary from mild infection to chronic infection and cancer. The white sucker hepatitis B virus (WSHBV) was first described in the white sucker (Catostomus commersonii), a freshwater teleost, and belongs to the genus Parahepadnavirus. At present, the host range of WSHBV and its impact on fish health are unknown, and neither genetic diversity nor association with fish health have been studied in any parahepadnavirus. Given the relevance of genomic diversity to disease outcome for the orthohepadnaviruses, we sought to characterize genomic variation in WSHBV and determine how it is structured among watersheds. We identified WSHBV-positive white sucker inhabiting tributaries of Lake Michigan, Lake Superior, Lake Erie (USA), and Lake Athabasca (Canada). Copy number in plasma and in liver tissue was estimated via qPCR. Templates from 27 virus-positive fish were amplified and sequenced using a primer-specific, circular long-range amplification method coupled with amplicon sequencing on the Illumina MiSeq. Phylogenetic analysis of the WSHBV genome identified phylogeographical clustering reminiscent of that observed with human hepatitis B virus genotypes. Notably, most non-synonymous substitutions were found to cluster in the pre-S/spacer overlap region, which is relevant for both viral entry and replication. The observed predominance of p1/s3 mutations in this region is indicative of adaptive change in the polymerase open reading frame (ORF), while, at the same time, the surface ORF is under purifying selection. Although the levels of variation we observed do not meet the criteria used to define sub/genotypes of human and avian hepadnaviruses, we identified geographically associated genome variation in the pre-S and spacer domain sufficient to define five WSHBV haplotypes. This study of WSHBV genetic diversity should facilitate the development of molecular markers for future identification of genotypes and provide evidence in future investigations of possible differential disease outcomes.


2021 ◽  
Vol 53 (1) ◽  
Author(s):  
Gabriele Senczuk ◽  
Salvatore Mastrangelo ◽  
Paolo Ajmone-Marsan ◽  
Zsolt Becskei ◽  
Paolo Colangelo ◽  
...  

Abstract Background During the Neolithic expansion, cattle accompanied humans and spread from their domestication centres to colonize the ancient world. In addition, European cattle occasionally intermingled with both indicine cattle and local aurochs resulting in an exclusive pattern of genetic diversity. Among the most ancient European cattle are breeds that belong to the so-called Podolian trunk, the history of which is still not well established. Here, we used genome-wide single nucleotide polymorphism (SNP) data on 806 individuals belonging to 36 breeds to reconstruct the origin and diversification of Podolian cattle and to provide a reliable scenario of the European colonization, through an approximate Bayesian computation random forest (ABC-RF) approach. Results Our results indicate that European Podolian cattle display higher values of genetic diversity indices than both African taurine and Asian indicine breeds. Clustering analyses show that Podolian breeds share close genomic relationships, which suggests a likely common genetic ancestry. Among the simulated and tested scenarios of the colonization of Europe from taurine cattle, the greatest support was obtained for the model assuming at least two waves of diffusion. Time estimates are in line with an early migration from the domestication centre of non-Podolian taurine breeds followed by a secondary migration of Podolian breeds. The best fitting model also suggests that the Italian Podolian breeds are the result of admixture between different genomic pools. Conclusions This comprehensive dataset that includes most of the autochthonous cattle breeds belonging to the so-called Podolian trunk allowed us not only to shed light onto the origin and diversification of this group of cattle, but also to gain new insights into the diffusion of European cattle. The most well-supported scenario of colonization points to two main waves of migrations: with one that occurred alongside with the Neolithic human expansion and gave rise to the non-Podolian taurine breeds, and a more recent one that favoured the diffusion of European Podolian. In this process, we highlight the importance of both the Mediterranean and Danube routes in promoting European cattle colonization. Moreover, we identified admixture as a driver of diversification in Italy, which could represent a melting pot for Podolian cattle.


Author(s):  
Gaotian Zhang ◽  
Jake D Mostad ◽  
Erik C Andersen

Abstract Life history traits underlie the fitness of organisms and are under strong natural selection. A new mutation that positively impacts a life history trait will likely increase in frequency and become fixed in a population (e.g. a selective sweep). The identification of the beneficial alleles that underlie selective sweeps provides insights into the mechanisms that occurred during the evolution of a species. In the global population of Caenorhabditis elegans, we previously identified selective sweeps that have drastically reduced chromosomal-scale genetic diversity in the species. Here, we measured the fecundity of 121 wild C. elegans strains, including many recently isolated divergent strains from the Hawaiian islands and found that strains with larger swept genomic regions have significantly higher fecundity than strains without evidence of the recent selective sweeps. We used genome-wide association (GWA) mapping to identify three quantitative trait loci (QTL) underlying the fecundity variation. Additionally, we mapped previous fecundity data from wild C. elegans strains and C. elegans recombinant inbred advanced intercross lines that were grown in various conditions and detected eight QTL using GWA and linkage mappings. These QTL show the genetic complexity of fecundity across this species. Moreover, the haplotype structure in each GWA QTL region revealed correlations with recent selective sweeps in the C. elegans population. North American and European strains had significantly higher fecundity than most strains from Hawaii, a hypothesized origin of the C. elegans species, suggesting that beneficial alleles that caused increased fecundity could underlie the selective sweeps during the worldwide expansion of C. elegans.


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