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

Abstract

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.

Invader at the edge — Genomic origins and physiological differences of round gobies across a steep urban salinity gradient

“…Furthermore, phenotypic differences attributed to local adaptation and environmental sorting based on phenotypic differences (albeit at much larger spatial scales) have previously been described for this species (Green et al, 2020;Green, Apostolou, et al, 2021).…”

“…The same was also true for MMR, which was consistently higher in the Outer port, regardless of salinity treatment. These subtle but evident physiological differences between sites may be attributed to long‐term ontogenetic acclimation (West‐Eberhard, 2003 ), genetic inheritance (Green, Apostolou, et al, 2021 ), or a combination of both (Czypionka et al, 2012 ). The adaptive benefits of higher MMR could potentially be explained by intraspecific ecology: more active and motile fish species have higher MMR compared to, for example, ambush predators (Norin & Clark, 2016 ).…”

“…These differences are based on differences in the environment, such as biotic toxins (Wendling & Mathias Wegner, 2015 ), salinity (Caputi et al, 2019 ; Chen et al, 2021 ; Green, Apostolou, et al, 2021 ; Renborg et al, 2014 ) and/or temperature refugia (Tepolt & Palumbi, 2015 ). During aquatic species invasions, these environmental factors also present physiological barriers and gradients that can shape the process by which a species establishes (Christensen et al, 2021 ; Green, Niemax, et al, 2021 ), evolves (Green, Apostolou, et al, 2021 ), spreads (Magellan et al, 2019 ) and interacts with other species in their surrounding environment (Moyle & Light, 1996 ).…”

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

“…To this end, advances in genomics are permitting genome‐wide scans and assessment of patterns of gene expression that in combination with common garden experiments, breeding experiments and quantitative genetic approaches are helping to identify candidate loci underpinning genetic adaptation and elucidate the genetic architecture of traits targeted by selection (Albecker et al, 2021 ). Of note, a recent study in the euryhaline round goby ( Neogobius melanostomus ) linked sperm performance in different salinities to population‐genomic patterns in Northern Europe (Green, Apostolou, et al, 2021 ). A similar approach might help to identify locally adapted C. signifera populations.…”

Ten years of marine evolutionary biology—Challenges and achievements of a multidisciplinary research initiative

“…This research also resulted in a new concept, ‘immigrant reproductive dysfunction’, as an important mechanism for reduced gene flow, local adaptation and speciation (Svensson et al, 2017 ). Investigations of a related but invasive species (round goby, Neogobius melanostomus ) focusing both on the genomic characterization (Adrian‐Kalchhauser et al, 2020 ) and on adaptation to increased salinities during its ongoing invasion of brackish and marine habitats, offered unique possibilities of studying local adaptation in real time (Green et al, 2019 , 2021 ).…”