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Genome analysis of the monoclonal marbled crayfish reveals genetic separation over a short evolutionary timescale.

ABSTRACT: The marbled crayfish (Procambarus virginalis) represents a very recently evolved parthenogenetic freshwater crayfish species that has invaded diverse habitats in Europe and in Madagascar. However, population genetic analyses have been hindered by the homogeneous genetic structure of the population and the lack of suitable tools for data analysis. We have used whole-genome sequencing to characterize reference specimens from various known wild populations. In parallel, we established a whole-genome sequencing data analysis pipeline for the population genetic analysis of nearly monoclonal genomes. Our results provide evidence for systematic genetic differences between geographically separated populations and illustrate the emerging differentiation of the marbled crayfish genome. We also used mark-recapture population size estimation in combination with genetic data to model the growth pattern of marbled crayfish populations. Our findings uncover evolutionary dynamics in the marbled crayfish genome over a very short evolutionary timescale and identify the rapid growth of marbled crayfish populations as an important factor for ecological monitoring.

SUBMITTER: Maiakovska O

PROVIDER: S-EPMC7814009 | biostudies-literature | 2021 Jan

REPOSITORIES: biostudies-literature

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Genome analysis of the monoclonal marbled crayfish reveals genetic separation over a short evolutionary timescale.

Maiakovska Olena O Andriantsoa Ranja R Tönges Sina S Legrand Carine C Gutekunst Julian J Hanna Katharina K Pârvulescu Lucian L Novitsky Roman R Weiperth András A Sciberras Arnold A Deidun Alan A Ercoli Fabio F Kouba Antonin A Lyko Frank F

Communications biology 20210118 1

The marbled crayfish (Procambarus virginalis) represents a very recently evolved parthenogenetic freshwater crayfish species that has invaded diverse habitats in Europe and in Madagascar. However, population genetic analyses have been hindered by the homogeneous genetic structure of the population and the lack of suitable tools for data analysis. We have used whole-genome sequencing to characterize reference specimens from various known wild populations. In parallel, we established a whole-genom ...[more]

PMID: 33462402

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Project description:Biological invasions are increasingly recognized ecological and economic threats to biodiversity and are projected to increase in the future. Introduced freshwater crayfish in particular are protruding invaders, exerting tremendous impacts on native biodiversity and ecosystem functioning, as exemplified by the North American spiny-cheek, signal and red swamp crayfish as well as the Australian common yabby. The marbled crayfish is among the most outstanding freshwater crayfish invaders due to its parthenogenetic reproduction combined with early maturation and high fecundity. As their introduced ranges expand, their sympatric populations become more frequent. The question of which species and under what circumstances will dominate in their introduced communities is of great interest to biodiversity conservation as it can offer valuable insights for understanding and prioritization of management efforts. In order to examine which of the aforementioned species may be more successful as an invader, we conducted a set of independent trials evaluating survival, growth, claw injury, and reproduction using single-species stocks (intraspecific interactions) and mixed stocks (interspecific interactions) of marbled crayfish vs. other crayfish invaders since the onset of exogenous feeding. In both single and mixed stocks, red swamp crayfish and yabby grew faster than marbled crayfish, while marbled crayfish were superior to both spiny-cheek and signal crayfish in terms of growth. With the exception of signal crayfish, the faster-growing species consistently reached a higher survival rate. The faster-growing species tended to negatively impair smaller counterparts by greater claw injury, delayed maturation, and reduced fecundity. Only marbled crayfish laid eggs as early as 14 weeks in this study, which is earlier than previously reported in the literature. Thus, the success of marbled crayfish among invasive crayfish is significantly driven by relatively fast growth as well as an early and frequent reproduction. These results shed light on how interactions between invasive populations can unfold when their expansion ranges overlap in the wild, thereby contributing to the knowledge base on the complex population dynamics between existing and emerging invasive species.

Project description:The invasion of the blacklegged tick, Ixodes scapularis into Ontario, Canada poses a significant risk to public health because it is a vector for numerous pathogens, including Borrelia burgdorferi sensu stricto, the causative agent of Lyme disease. Baseline field sampling in 2014 and 2015 detected I. scapularis and B. burgdorferi at sites across southern, eastern and central Ontario, including a hot spot in eastern Ontario. A "speed of spread" model for I. scapularis developed by Leighton and colleagues (2012) estimated that the tick's range was expanding northward at 46 km/year. In 2016, we revisited a subset of sites sampled in 2014 and 2015 to understand the changing nature of risk, and assess whether the rate of tick invasion is consistent with the speed of spread estimate. Ticks were collected via tick dragging at 17 out of 36 sites, 5 of which were new sites for I. scapularis. Samples were positive for B. burgdorferi at 8 sites. No other I. scapularis-borne pathogens were detected. Centrographic statistics revealed an increase in the dispersion of I. scapularis positive sites in eastern Ontario. Field data for each site were then compared to the model's predicted year of establishment for each census subdivision. Our findings illustrate that the range expansion of I. scapularis and the emergence of B. burgdorferi is ongoing, and provide short timescale evidence of the processes associated with I. scapularis spread. The range front appears to be moving at a rate of ~46 km/year, with colonization of the tick behind this range front occurring at a slower and heterogeneous rate. Assessment of site-level ecological factors did not provide any insight into the underlying processes that may be influencing the colonization of I. scapularis in specific areas. Ongoing field sampling is needed to monitor this dynamic process. This study highlights the current geographic risk associated with Lyme disease, which can be used to target public health interventions to the areas of greatest risk.

Dataset Information

Genome analysis of the monoclonal marbled crayfish reveals genetic separation over a short evolutionary timescale.

Publications

Genome analysis of the monoclonal marbled crayfish reveals genetic separation over a short evolutionary timescale.

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