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

Leon Green,Charlotta Kvarnemo,Kajsa Palmqvist,Jane W Behrens,Jonathan N Havenhand,Erica H Leder,Apostolos Apostolou,Ellika Faust

doi:10.3390/cells10071743

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.

Highlights

Since the onset of Parker’s development of sperm evolutionary theories in the 1970’s, the understanding of and research on gamete evolution has increased dramatically [2,3,4]
Given that the round goby is invasive in a broad range of salinities [33,67], it is imperative to understand how the ancestral origin of the species contributes to their ability to reproduce within their introduced range
Despite the difference in genetic diversity, our results clearly show that freshwater ecotypes are more closely related to each other than to brackish ecotypes, and that they share similar phenotypic responses in their sperm when tested across the sampled salinities

Summary

Introduction

Since the onset of Parker’s development of sperm evolutionary theories in the 1970’s (most notably Parker 1970 [1]), the understanding of and research on gamete evolution has increased dramatically [2,3,4]. A few species that can reproduce across a wide range of salinities are able to respond plastically to the environment and produce sperm that are triggered to swim in the salinity in which the males have been spending the last days or months (depending on species) [24,25,26]. Several of these fishes have the status of non-indigenous species (NIS), such as the killifish [26] and Tilapia spp. Several of these fishes have the status of non-indigenous species (NIS), such as the killifish [26] and Tilapia spp. [25]

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Conclusion