Threespine Stickleback in Lake Constance: The Ecology and Genomic Substrate of a Recent Invasion

Invasive species can be powerful models for studying contemporary evolution in natural environments. As invading organisms often encounter new habitats during colonization, they will experience novel selection pressures. Threespine stickleback (Gasterosteus aculeatus complex) have recently colonized large parts of Switzerland and are invasive in Lake Constance. Introduced to several watersheds roughly 150 years ago, they spread across the Swiss Plateau (400–800 m a.s.l.), bringing three divergent hitherto allopatric lineages into secondary contact. As stickleback have colonized a variety of different habitat types during this recent range expansion, the Swiss system is a useful model for studying contemporary evolution with and without secondary contact. For example, in the Lake Constance region there has been rapid phenotypic and genetic divergence between a lake population and some stream populations. There is considerable phenotypic variation within the lake population, with individuals foraging in and occupying littoral, offshore pelagic, and profundal waters, the latter of which is a very unusual habitat for stickleback. Furthermore, adults from the lake population can reach up to three times the size of adults from the surrounding stream populations, and are large by comparison to populations globally. Here, we review the historical origins of the threespine stickleback in Switzerland, and the ecomorphological variation and genomic basis of its invasion in Lake Constance. We also outline the potential ecological impacts of this invasion, and highlight the interest for contemporary evolution studies.

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Elevated temperatures drive the evolution of armor loss in the threespine stickleback Gasterosteus aculeatus

10.1101/2020.10.29.361568 ◽

2020 ◽

Author(s):

Carl Smith ◽

Grzegorz Zięba ◽

Mirosław Przybylski

Keyword(s):

Genetic Basis ◽

Gasterosteus Aculeatus ◽

Elevated Temperatures ◽

Population Level ◽

Functional Trait ◽

Threespine Stickleback ◽

Ecological Impacts ◽

Correlated Response ◽

Reduced Body ◽

Bayesian Spatial Model

AbstractWhile there is evidence of genetic and phenotypic responses to climate change, few studies have demonstrated change in functional traits with a known genetic basis. Here we present evidence for an evolutionary adaptive response to elevated temperatures in freshwater populations of the threespine stickleback (Gasterosteus aculeatus). Using a unique set of historical data and museum specimens, in combination with contemporary samples, we fitted a Bayesian spatial model to identify a population-level decline in the number of lateral bony plates, comprising anti-predator armor, in multiple populations of sticklebacks over the last 90 years in Poland. Armor loss was predicted by elevated temperatures and is proposed to be a correlated response to selection for reduced body size. This study demonstrates a change in a functional trait of known genetic basis in response to elevated temperature, and illustrates the utility of the threespine stickleback as a model for measuring the evolutionary and ecological impacts of environmental change across the northern hemisphere.

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Diversity and sexual dimorphism in the head lateral line system in North Sea populations of threespine sticklebacks, Gasterosteus aculeatus (Teleostei: Gasterosteidae)

Zoomorphology ◽

10.1007/s00435-020-00513-1 ◽

2020 ◽

Author(s):

Harald Ahnelt ◽

David Ramler ◽

Maria Ø. Madsen ◽

Lasse F. Jensen ◽

Sonja Windhager

Keyword(s):

Sexual Dimorphism ◽

North Sea ◽

Lateral Line ◽

Gasterosteus Aculeatus ◽

Sensory System ◽

Threespine Stickleback ◽

Lateral Line System ◽

Line System ◽

Marine Population ◽

Threespine Sticklebacks

AbstractThe mechanosensory lateral line of fishes is a flow sensing system and supports a number of behaviors, e.g. prey detection, schooling or position holding in water currents. Differences in the neuromast pattern of this sensory system reflect adaptation to divergent ecological constraints. The threespine stickleback, Gasterosteus aculeatus, is known for its ecological plasticity resulting in three major ecotypes, a marine type, a migrating anadromous type and a resident freshwater type. We provide the first comparative study of the pattern of the head lateral line system of North Sea populations representing these three ecotypes including a brackish spawning population. We found no distinct difference in the pattern of the head lateral line system between the three ecotypes but significant differences in neuromast numbers. The anadromous and the brackish populations had distinctly less neuromasts than their freshwater and marine conspecifics. This difference in neuromast number between marine and anadromous threespine stickleback points to differences in swimming behavior. We also found sexual dimorphism in neuromast number with males having more neuromasts than females in the anadromous, brackish and the freshwater populations. But no such dimorphism occurred in the marine population. Our results suggest that the head lateral line of the three ecotypes is under divergent hydrodynamic constraints. Additionally, sexual dimorphism points to divergent niche partitioning of males and females in the anadromous and freshwater but not in the marine populations. Our findings imply careful sampling as an important prerequisite to discern especially between anadromous and marine threespine sticklebacks.

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Seasonal changes in carotenoid and lipid storage by threespine stickleback, Gasterosteus aculeatus

Environmental Biology of Fishes ◽

10.1007/s10641-013-0130-x ◽

2013 ◽

Vol 97 (2) ◽

pp. 209-214 ◽

Cited By ~ 9

Author(s):

C. A. Black ◽

R. J. Scott ◽

M. A. Bernards

Keyword(s):

Seasonal Changes ◽

Gasterosteus Aculeatus ◽

Threespine Stickleback ◽

Lipid Storage

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Responses of threespine stickleback (Gasterosteus aculeatus, L) transcriptome to hypoxia

Comparative Biochemistry and Physiology Part D Genomics and Proteomics ◽

10.1016/j.cbd.2011.08.001 ◽

2011 ◽

Vol 6 (4) ◽

pp. 370-381 ◽

Cited By ~ 17

Author(s):

L. Leveelahti ◽

P. Leskinen ◽

E.H. Leder ◽

W. Waser ◽

M. Nikinmaa

Keyword(s):

Gasterosteus Aculeatus ◽

Threespine Stickleback

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Heritability of DNA methylation in threespine stickleback (Gasterosteus aculeatus)

Genetics ◽

10.1093/genetics/iyab001 ◽

2021 ◽

Vol 217 (1) ◽

Author(s):

Juntao Hu ◽

Sara J S Wuitchik ◽

Tegan N Barry ◽

Heather A Jamniczky ◽

Sean M Rogers ◽

...

Keyword(s):

Dna Methylation ◽

Genetic Architecture ◽

Gasterosteus Aculeatus ◽

Additive Genetic Variance ◽

Natural Populations ◽

Threespine Stickleback ◽

Phenotypic Change ◽

Cpg Sites ◽

Cis And Trans ◽

Methylation Variation

Abstract Epigenetic mechanisms underlying phenotypic change are hypothesized to contribute to population persistence and adaptation in the face of environmental change. To date, few studies have explored the heritability of intergenerationally stable methylation levels in natural populations, and little is known about the relative contribution of cis- and trans-regulatory changes to methylation variation. Here, we explore the heritability of DNA methylation, and conduct methylation quantitative trait loci (meQTLs) analysis to investigate the genetic architecture underlying methylation variation between marine and freshwater ecotypes of threespine stickleback (Gasterosteus aculeatus). We quantitatively measured genome-wide DNA methylation in fin tissue using reduced representation bisulfite sequencing of F1 and F2 crosses, and their marine and freshwater source populations. We identified cytosines (CpG sites) that exhibited stable methylation levels across generations. We found that additive genetic variance explained an average of 24–35% of the methylation variance, with a number of CpG sites possibly autonomous from genetic control. We also detected both cis- and trans-meQTLs, with only trans-meQTLs overlapping with previously identified genomic regions of high differentiation between marine and freshwater ecotypes. Finally, we identified the genetic architecture underlying two key CpG sites that were differentially methylated between ecotypes. These findings demonstrate a potential role for DNA methylation in facilitating adaptation to divergent environments and improve our understanding of the heritable basis of population epigenomic variation.

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Purification and Properties of the Threespine Stickleback (Gasterosteus aculeatus) Lactate Dehydrogenase LDH-B4 and LDH-C4 Isoenzymes

Comparative Biochemistry and Physiology Part B Biochemistry and Molecular Biology ◽

10.1016/s0305-0491(97)00003-5 ◽

1997 ◽

Vol 117 (4) ◽

pp. 571-577 ◽

Cited By ~ 1

Author(s):

Marek S. Ziętara ◽

Jadwiga Gronczewska ◽

Edward F. Skorkowski

Keyword(s):

Lactate Dehydrogenase ◽

Gasterosteus Aculeatus ◽

Threespine Stickleback ◽

Purification And Properties

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Introduction and Spread of the Threespine Stickleback (Gasterosteus Aculeatus) in Lakes Huron and Michigan

Journal of Great Lakes Research ◽

10.1016/s0380-1330(85)71794-7 ◽

1985 ◽

Vol 11 (4) ◽

pp. 508-511 ◽

Cited By ~ 10

Author(s):

Ralph M. Stedman ◽

Charles A. Bowen

Keyword(s):

Gasterosteus Aculeatus ◽

Threespine Stickleback

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Host mortality and variability in epizootics of Schistocephalus solidus infecting the threespine stickleback, Gasterosteus aculeatus

Parasitology ◽

10.1017/s003118201000048x ◽

2010 ◽

Vol 137 (11) ◽

pp. 1681-1686 ◽

Cited By ~ 21

Author(s):

D. C. HEINS ◽

E. L. BIRDEN ◽

J. A. BAKER

Keyword(s):

Gasterosteus Aculeatus ◽

Infected Fish ◽

Threespine Stickleback ◽

Intensity Of Infection ◽

Host Fish ◽

Schistocephalus Solidus ◽

Second Intermediate Host ◽

Host Mortality ◽

Abiotic And Biotic Factors ◽

Host Behaviour

SUMMARYAn analysis of the metrics of Schistocephalus solidus infection of the threespine stickleback, Gasterosteus aculeatus, in Walby Lake, Alaska, showed that an epizootic ended between 1996 and 1998 and another occurred between 1998 and 2003. The end of the first epizootic was associated with a crash in population size of the stickleback, which serves as the second intermediate host. The likely cause of the end of that epizootic is mass mortality of host fish over winter in 1996–1997. The deleterious impact of the parasite on host reproduction and increased host predation associated with parasitic manipulation of host behaviour and morphology to facilitate transmission might also have played a role, along with unknown environmental factors acting on heavily infected fish or fish in poor condition. The second epizootic was linked to relatively high levels of prevalence and mean intensity of infection, but parasite:host mass ratios were quite low at the peak and there were no apparent mass deaths of the host. A number of abiotic and biotic factors are likely to interact to contribute to the occurrence of epizootics in S. solidus, which appear to be unstable and variable. Epizootics appear to depend on particular and, at times, rare sets of circumstances.

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Comparison of the fast-start performances of closely related, morphologically distinct threespine sticklebacks (Gasterosteus spp.)

Journal of Experimental Biology ◽

10.1242/jeb.199.12.2595 ◽

1996 ◽

Vol 199 (12) ◽

pp. 2595-2604 ◽

Cited By ~ 5

Author(s):

T Law ◽

R Blake

Keyword(s):

Angular Velocity ◽

High Speed ◽

High Performance ◽

Gasterosteus Aculeatus ◽

Morphological Characteristics ◽

Maximum Velocity ◽

Threespine Stickleback ◽

Biomechanical Study ◽

Maximum Acceleration ◽

Fast Start

Fast-start escape performances for two species of threespine stickleback, Gasterosteus spp., were investigated using high-speed cinematography (400 Hz). The two fishes (not yet formally described, referred to here as benthic and limnetic) inhabit different niches within Paxton Lake, British Columbia, Canada, and are recent, morphologically distinct species. All escape responses observed for both species were double-bend C-type fast-starts. There were no significant differences between the species for any linear or angular parameter (pooled averages, both species: duration 0.048 s, distance 0.033 m, maximum velocity 1.10 m s-1, maximum acceleration 137 m s-2, maximum horizontal angular velocity 473.6 rad s-1 and maximum overall angular velocity 511.1 rad s-1). Benthics and limnetics have the greatest added mass (Ma) at 0.3 and 0.6 body lengths, respectively. The maximum Ma does not include the fins for benthics, but for limnetics the dorsal and anal fins contribute greatly to the maximum Ma. The deep, posteriorly placed fins of limnetics enable them to have a fast-start performance equivalent to that of the deeper-bodied benthics. Both the limnetic and benthic fishes have significantly higher escape fast-start velocities than their ancestral form, the anadromous threespine stickleback Gasterosteus aculeatus, suggesting that the high performance of the Paxton Lake sticklebacks is an evolutionarily derived trait. In this biomechanical study of functional morphology, we demonstrate that similar high fast-start performance can be achieved by different suites of morphological characteristics and suggest that predation might be the selective force for the high escape performance in these two fishes.

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