Sperm performance limits the reproduction of an invasive fish in novel salinities

Green, León; Niemax, Jan; Herrmann, Jens-Peter; Temming, Axel; Behrens, Jane; Havenhand, Jonathan N.; Leder, Erica H.; Kvarnemo, Charlotta

doi:10.1111/ddi.13258

Cited by 9 publications

(22 citation statements)

References 84 publications

(124 reference statements)

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“…While invasion routes are difficult to uncover, our study shows that reproductive traits of introduced round gobies can be tightly linked to the ancestral, locally adapted ecotypes and the population genomics of the species. Similar to the previous study published by Green, Niemax et al in 2021 [ 38 ], our results show that round gobies with a freshwater ancestry had comparatively low sperm performance in brackish or marine conditions, which may limit these genotypes to freshwater environments. Gobies with a brackish genetic ancestry had the best sperm performance in brackish conditions and are therefore likely to be better able to reproduce in these salinities.…”

Section: Discussionsupporting

confidence: 91%

“…Round gobies can reproduce under sperm competition [ 89 ], and sneaker morph males have been found in both freshwater [ 42 ] and brackish environments [ 38 ]. Due to the limits of our fishing methods (cage mesh size: 20 mm, and hook size: 10–14 mm), we are unlikely to have caught any of the potential minute sneaker males previously reported by Marentette et al [ 42 ].…”

Section: Discussionmentioning

confidence: 99%

“…Sperm measurements were performed following the same protocol as used in the previous studies to which they were to be compared against ([ 35 , 38 , 39 ]; Table 1 ). Fourteen males caught in Danube (freshwater origin, 0 PSU: N = 14) and twelve males caught near Sozopol on the Bulgarian coast (brackish origin, ~16 PSU: N = 12) were kept in aerated tanks with water from their site of capture for less than 7 days, before they were sampled for sperm data at the Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences’ Laboratory of Marine Ecology, Sozopol, Bulgaria.…”

Section: Methodsmentioning

confidence: 99%

“…Data on sperm motility and sperm velocity tested in freshwater (0 or 1 PSU), brackish (15 or 16 PSU) and marine (30 or 32 PSU) salinities were collected for a total of nine sites from three previously published sources where raw data were available (Green, Havenhand, et al, 2020 [ 39 ], Green, Niemax, et al, 2020 [ 35 ], 2021 [ 38 ]). See Table 1 for details on each site and test salinities.…”

Section: Methodsmentioning

confidence: 99%

“…Theory predicts that selection on sperm in the round goby is strong, since they often reproduce under sperm competition, and detrimental environmental conditions may cause sperm limitation [ 35 , 36 , 37 ]. Recent studies suggest that the round goby is incapable of acclimating their sperm performance to match novel salinity conditions [ 38 ], but there is support for local adaptation in its sperm traits [ 39 ]. This has raised the hypothesis that reproduction in widely different environments may be possible due to different ancestral origins of the populations that are now spreading in different aquatic environments within Europe and North America.…”

Section: Introductionmentioning

confidence: 99%

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Ancestral Sperm Ecotypes Reveal Multiple Invasions of a Non-Native Fish in Northern Europe

Green

Apostolou

Faust

et al. 2021

Cells

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For externally fertilising organisms in the aquatic environment, the abiotic fertilisation medium can be a strong selecting force. Among bony fishes, sperm are adapted to function in a narrow salinity range. A notable exception is the family Gobiidae, where several species reproduce across a wide salinity range. The family also contains several wide-spread invasive species. To better understand how these fishes tolerate such varying conditions, we measured sperm performance in relation to salinity from a freshwater and a brackish population within their ancestral Ponto-Caspian region of the round goby, Neogobius melanostomus. These two ancestral populations were then compared to nine additional invaded sites across northern Europe, both in terms of their sperm traits and by using genomic SNP markers. Our results show clear patterns of ancestral adaptations to freshwater and brackish salinities in their sperm performance. Population genomic analyses show that the ancestral ecotypes have generally established themselves in environments that fit their sperm adaptations. Sites close to ports with intense shipping show that both outbreeding and admixture can affect the sperm performance of a population in a given salinity. Rapid adaptation to local conditions is also supported at some sites. Historical and contemporary evolution in the traits of the round goby sperm cells is tightly linked to the population and seascape genomics as well as biogeographic processes in these invasive fishes. Since the risk of a population establishing in an area is related to the genotype by environment match, port connectivity and the ancestry of the round goby population can likely be useful for predicting the species spread.

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Section: Discussionsupporting

confidence: 91%

Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Ancestral Sperm Ecotypes Reveal Multiple Invasions of a Non-Native Fish in Northern Europe

Green

Apostolou

Faust

et al. 2021

Cells

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A test for plasticity in sperm motility activation in response to osmotic environment in an anuran amphibian

Byrne

Anastas

Silla

2022

Ecology and Evolution

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Evolutionary theory predicts that selection will favor phenotypic plasticity in sperm traits that maximize fertilization success in dynamic fertilization environments. In species with external fertilization, osmolality of the fertilization medium is known to play a critical role in activating sperm motility, but evidence for osmotic‐induced sperm plasticity is limited to euryhaline fish and marine invertebrates. Whether this capacity extends to freshwater taxa remains unknown. Here, we provide the first test for plasticity in sperm‐motility activation in response to osmotic environment in an anuran amphibian. Male common eastern froglets ( Crinia signifera ) were acclimated to either low (0 mOsmol kg −1 ) or high (50 mOsmol kg −1 ) environmental osmolality, and using a split‐sample experimental design, sperm were activated across a range of osmolality treatments (0, 25, 50, 75, 100, and 200 ± 2 mOsmol kg −1 ). Unexpectedly, there was no detectable shift in the optimal osmolality for sperm‐motility activation after approximately 13 weeks of acclimation (a period reflecting the duration of the winter breeding season). However, in both the low and high acclimation treatments, the optimal osmolality for sperm‐motility activation mirrored the osmolality at the natural breeding site, indicating a phenotypic match to the local environment. Previously it has been shown that C. signifera display among‐population covariation between environmental osmolality and sperm performance. Coupled with this finding, the results of the present study suggest that inter‐population differences reflect genetic divergence and local adaptation. We discuss the need for experimental tests of osmotic‐induced sperm plasticity in more freshwater taxa to better understand the environmental and evolutionary contexts favoring adaptive plasticity in sperm‐motility activation.

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Identifying high-risk areas for introduction of new alien species: the case of the invasive round goby, a door-knocker for Norway

Forsgren

Hanssen

2022

Hydrobiologia

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Identifying new areas of colonisation by alien species is important for early detection and management. Door-knocker species pose problems for traditional predictive models because of lacking presence–absence data, but habitat suitability modelling might overcome this. We here identify the most likely areas for introduction and first establishment of the invasive round goby Neogobius melanostomus to Norway, where it has not yet been registered. We implemented knowledge on dispersal pathways and the species’ biology in a simplified suitability model based on spatial data representing the most relevant environmental variables: distance to international harbours in Norway, distance to the closest population in neighbouring country, salinity, wave exposure, depth and water temperature. The results suggest that there are many potential localities for introduction and first establishment and reveal several hotspots of such areas, especially in less-exposed coastal brackish areas of southern Norway. Especially the region around the Oslo Fjord stands out as being associated with higher risk. Our results could guide future monitoring programmes and increase the chance of early detection of this potential new invader. The study illustrates how spatial analyses can be used to identify the most likely areas for future invasion by an aquatic door-knocker species despite lacking presence–absence data.

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Sperm performance limits the reproduction of an invasive fish in novel salinities

Abstract: This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Cited by 9 publications

References 84 publications

Ancestral Sperm Ecotypes Reveal Multiple Invasions of a Non-Native Fish in Northern Europe

Ancestral Sperm Ecotypes Reveal Multiple Invasions of a Non-Native Fish in Northern Europe

A test for plasticity in sperm motility activation in response to osmotic environment in an anuran amphibian

Identifying high-risk areas for introduction of new alien species: the case of the invasive round goby, a door-knocker for Norway

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