Evidence of rapid adaptive trait change to local salinity in the sperm of an invasive fish

Abstract

Invasive species may quickly colonize novel environments, which could be attributed to both phenotypic plasticity and an ability to locally adapt. Reproductive traits are expected to be under strong selection when the new environment limits reproductive success of the invading species. This may be especially important for external fertilizers, which release sperm and eggs into the new environment. Despite adult tolerance to high salinity, the invasive fish Neogobius melanostomus (round goby) is absent from fully marine regions of the Baltic Sea, raising the possibility that its distribution is limited by tolerance during earlier life stages. Here, we investigate the hypothesis that the spread of N. melanostomus is limited by sperm function in novel salinities. We sampled sperm from two invasion fronts with higher and lower salinities in the Baltic Sea and tested them across a range of salinity levels. We found that sperm velocity and percentage of motile sperm declined in salinity levels higher and lower than those currently experienced by the Baltic Sea populations, with different performance curves for the two fronts. Sperm velocity also peaked closer to the home salinity conditions in each respective invasion front, with older localities showing an increased fit to local conditions. By calculating how the sperm velocity has changed over generations, we show this phenotypic shift to be in the range of other fish species under strong selection, indicating ongoing local adaptation or epigenetic acclimation to their novel environment. These results show that while immigrant reproductive dysfunction appears to at least partly limit the distribution of invasive N. melanostomus in the Baltic Sea, local adaptation to novel environments could enable future spread beyond their current boundaries.

Alternative reproductive tactics are associated with sperm performance in invasive round goby from two different salinity environments

“…The three drops, placed on the same slide, were immediately filmed in rapid succession using a camera (PixeLINK PL-D725, Pixelink, Ottawa, Canada) fitted to a microscope (same as above) with a 10× magnification objective and standard contrast and illumination, for 15 frames (frame rate: 30 frames/s, size: 2,592 × 2,048 pixels, exposure time: 10 ms, gain: 0, gamma: 0.1). Analysis of the videos was done through the computer-assisted sperm analysis (CASA) plugin (Wilson-Leedy & Ingermann, 2007) for ImageJ (National Institutes of Health, Bethesda, MD, USA) following standard procedures (Purchase & Earle, 2012) and CASA settings reported in the supplementary information in Green et al (2020). The sperm velocity parameter chosen was velocity of the curvilinear path (VCL) to allow for comparison with previous studies (Green et al, 2020;Marentette et al, 2009).…”

“…Analysis of the videos was done through the computer-assisted sperm analysis (CASA) plugin (Wilson-Leedy & Ingermann, 2007) for ImageJ (National Institutes of Health, Bethesda, MD, USA) following standard procedures (Purchase & Earle, 2012) and CASA settings reported in the supplementary information in Green et al (2020). The sperm velocity parameter chosen was velocity of the curvilinear path (VCL) to allow for comparison with previous studies (Green et al, 2020;Marentette et al, 2009). Since the procedure was replicated, the velocity measurements from each of the three technical replicates were used to calculate an average for each male and treatment condition.…”

“…We sampled fish from a population in a brackish estuary in the southern Baltic Sea (estimated to be 11 years old at the time of sampling) and the river Elbe (estimated to be 9 years old) (Hempel & Thiel, 2013). Since the round goby has its evolutionary history in brackish water, and sperm performance has been reported to decline in lower salinities (Green et al, 2020), we hypothesize that (I) sperm viability is lower in freshwater, but that this effect is ameliorated by ejaculate components from the SDGs. As a consequence of this, we hypothesize that (II) males living in fresh water invest more in SDG content to increase sperm viability.…”

Estimating salinity stress via hsp70 expression in the invasive round goby (Neogobius melanostomus): implications for further range expansion

“…Further spread of this invasive species into the saline North Sea will likely also be regulated by a combination of the physiological tolerance and phenotypic plasticity of the likely most vulnerable life stages of the species, i.e. eggs and larvae (Green et al, 2019), by abiotic and biotic interactions (e.g. competition/predation), as well as the species' potential for expanding their range through genetically adapting to higher salinities.…”

“…This was supported by an experiment showing that metabolic and osmoregulatory performance and survival are reduced under high salinities (30, and to some extent at salinity 25) compared to salinities 0-20 (Behrens et al, 2017). It is possible that although adult N. melanostomus often tolerate a wide range of abiotic conditions, reproduction, survival, and early life stage growth of populations may be restricted under high salinity (see Green et al, 2019), leading to decreased invasion potential further north-westward into the fully oceanic North Sea (Behrens et al, 2017). Potential phenotypic plasticity in stress tolerance, however, might aid its populations in survival and establishment in novel, suboptimal environments (Moran & Alexander, 2014), and drive differentiation of the round goby Fig.…”