Anthropogenic noise disrupts early-life development in a fish with paternal care.

Anthropogenic noise is a global pollutant but its potential impacts on early life-stages in fishes are largely unknown. Here, using controlled laboratory experiments, we tested for impacts of continuous or intermittent exposure to low-frequency broadband noise on early life-stages of the common goby (Pomatoschistus microps), a marine fish with exclusive paternal care. Neither continuous nor intermittent noise exposure had an effect on filial cannibalism, showing that males were capable and willing to care for their broods. However, broods reared in continuous noise covered a smaller area and contained fewer eggs than control broods. Moreover, although developmental rate was the same in all treatments, larvae reared by males in continuous noise had, on average, a smaller yolk sac at hatching than those reared in the intermittent noise and control treatments, while larvae body length did not differ. Thus, it appears that the increased consumption of the yolk sac reserve was not utilised for increased growth. This suggests that exposure to noise in early life-stages affects fitness-related traits of surviving offspring, given the crucial importance of the yolk sac reserve during the early life of pelagic larvae. More broadly, our findings highlight the wide-ranging impacts of anthropogenic noise on aquatic wildlife living in an increasingly noisy world.

Mating competition among females: testing the distinction between natural and sexual selection in an insect.

In species where females compete for mates, the male often provides the female with resources in addition to gametes. A recently suggested definition of sexual selection proposed that if females only benefit from additional resources that come with each mating and not additional gametes, female intrasexual competition for mating opportunities would result in natural selection rather than sexual selection. The nuptial gift-giving bushcricket Kawanaphila nartee has dynamic sex roles and has been a textbook example of sexual selection acting on females via mating competition. We investigated whether females of this species gain fitness benefits from nuptial gifts, additional ejaculates or both by controlling the number of matings and whether the female was allowed to consume the nutritious gift (spermatophylax) at mating. We found that egg production per day of life increased with the number of additional matings, both with and without spermatophylax consumption, but consuming the spermatophylax had an additional positive effect on the number of eggs. These effects were particularly strong in females with shorter lifespans. We discuss how the recently suggested definition of sexual selection applies to nuptial-feeding insects and conclude that both natural and sexual selections influence mating competition in K. nartee females.

How sexual and natural selection interact and shape the evolution of nests and nesting behaviour in fishes.

Among ray-finned fishes that provide parental care, many spawn in constructed nests, ranging from bowls, burrows and ridges to nests made of algae or bubbles. Because a nest by definition is a construction that enhances the nest-builder's fitness by helping it meet the needs of the developing offspring, nest-building behaviour is naturally selected, as is a preference for spawning with mates that provide well-built nests. However, nest-building behaviour can also be sexually selected, when nest traits increase mating success, protect against sperm competition or nest take-overs by conspecifics. Here, we offer a systematic review, with examples of how competition for sites and location of fish nests relates to sexual selection. We examine direct and indirect benefits of mate choice linked to nest traits, and different types of nests, from a sexual selection perspective. Nest-related behaviours are often under both natural and sexual selection, and we disentangle examples where that is the case, with special attention to females. We highlight some taxa in which nest building is likely to be sexually selected, but lack of research has left them uninvestigated. Some of them are established aquarium species, making them particularly amenable for future research. Finally, we compare with arthropods, amphibians and birds. This article is part of the theme issue 'The evolutionary ecology of nests: a cross-taxon approach'.

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

The Centre for Marine Evolutionary Biology (CeMEB) at the University of Gothenburg, Sweden, was established in 2008 through a 10-year research grant of 8.7 m€ to a team of senior researchers. Today, CeMEB members have contributed >500 scientific publications, 30 PhD theses and have organised 75 meetings and courses, including 18 three-day meetings and four conferences. What are the footprints of CeMEB, and how will the centre continue to play a national and international role as an important node of marine evolutionary research? In this perspective article, we first look back over the 10 years of CeMEB activities and briefly survey some of the many achievements of CeMEB. We furthermore compare the initial goals, as formulated in the grant application, with what has been achieved, and discuss challenges and milestones along the way. Finally, we bring forward some general lessons that can be learnt from a research funding of this type, and we also look ahead, discussing how CeMEB's achievements and lessons can be used as a springboard to the future of marine evolutionary biology.

Molecular, behavioural and morphological comparisons of sperm adaptations in a fish with alternative reproductive tactics.

In species with alternative reproductive tactics, there is much empirical support that parasitically spawning males have larger testes and greater sperm numbers as an evolved response to a higher degree of sperm competition, but support for higher sperm performance (motility, longevity and speed) by such males is inconsistent. We used the sand goby (Pomatoschistus minutus) to test whether sperm performance differed between breeding-coloured males (small testes, large mucus-filled sperm-duct glands; build nests lined with sperm-containing mucus, provide care) and parasitic sneaker-morph males (no breeding colouration, large testes, rudimentary sperm-duct glands; no nest, no care). We compared motility (per cent motile sperm), velocity, longevity of sperm, gene expression of testes and sperm morphometrics between the two morphs. We also tested if sperm-duct gland contents affected sperm performance. We found a clear difference in gene expression of testes between the male morphs with 109 transcripts differentially expressed between the morphs. Notably, several mucin genes were upregulated in breeding-coloured males and two ATP-related genes were upregulated in sneaker-morph males. There was a partial evidence of higher sperm velocity in sneaker-morph males, but no difference in sperm motility. Presence of sperm-duct gland contents significantly increased sperm velocity, and nonsignificantly tended to increase sperm motility, but equally so for the two morphs. The sand goby has remarkably long-lived sperm, with only small or no decline in motility and velocity over time (5 min vs. 22 h), but again, this was equally true for both morphs. Sperm length (head, flagella, total and flagella-to-head ratio) did not differ between morphs and did not correlate with sperm velocity for either morph. Thus, other than a clear difference in testes gene expression, we found only modest differences between the two male morphs, confirming previous findings that increased sperm performance as an adaptation to sperm competition is not a primary target of evolution.

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

Species invasions are a global problem of increasing concern, especially in highly connected aquatic environments. Despite this, salinity conditions can pose physiological barriers to their spread, and understanding them is important for management. In Scandinavia's largest cargo port, the invasive round goby (Neogobius melanostomus) is established across a steep salinity gradient. We used 12,937 SNPs to identify the genetic origin and diversity of three sites along the salinity gradient and round goby from western, central and northern Baltic Sea, as well as north European rivers. Fish from two sites from the extreme ends of the gradient were also acclimated to freshwater and seawater, and tested for respiratory and osmoregulatory physiology. Fish from the high-salinity environment in the outer port showed higher genetic diversity, and closer relatedness to the other regions, compared to fish from lower salinity upstream the river. Fish from the high-salinity site also had higher maximum metabolic rate, fewer blood cells and lower blood Ca2+. Despite these genotypic and phenotypic differences, salinity acclimation affected fish from both sites in the same way: seawater increased the blood osmolality and Na+ levels, and freshwater increased the levels of the stress hormone cortisol. Our results show genotypic and phenotypic differences over short spatial scales across this steep salinity gradient. These patterns of the physiologically robust round goby are likely driven by multiple introductions into the high-salinity site, and a process of sorting, likely based on behaviour or selection, along the gradient. This euryhaline fish risks spreading from this area, and seascape genomics and phenotypic characterization can inform management strategies even within an area as small as a coastal harbour inlet.

The definition of sexual selection.

Sexual selection is a key component of evolutionary biology. However, from the very formulation of sexual selection by Darwin, the nature and extent of sexual selection have been controversial. Recently, such controversy has led back to the fundamental question of just what sexual selection is. This has included how we incorporate female-female reproductive competition into sexual or natural selection. In this review, we do four things. First, we examine what we want a definition to do. Second, we define sexual selection: sexual selection is any selection that arises from fitness differences associated with nonrandom success in the competition for access to gametes for fertilization. An important outcome of this is that as mates often also offer access to resources, when those resources are the targets of the competition, rather than their gametes, the process should be considered natural rather than sexual selection. We believe this definition encapsulates both much of Darwin's original thinking about sexual selection, and much of how contemporary biologists use the concept of sexual selection. Third, we address alternative definitions, focusing in some detail on the role of female reproductive competition. Fourth, we challenge our definition with a number of scenarios, for instance where natural and sexual selection may align (as in some forms of endurance rivalry), or where differential allocation means teasing apart how fecundity and access to gametes influence fitness. In conclusion, we emphasize that whilst the ecological realities of sexual selection are likely to be complex, the definition of sexual selection is rather simple.

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

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.

Sperm adaptation in relation to salinity in three goby species.

In externally fertilizing species, the gametes of both males and females are exposed to the influences of the environment into which they are released. Sperm are sensitive to abiotic factors such as salinity, but they are also affected by biotic factors such as sperm competition. In this study, the authors compared the performance of sperm of three goby species, the painted goby, Pomatoschistus pictus, the two-spotted goby, Pomatoschistus flavescens, and the sand goby, Pomatoschistus minutus. These species differ in their distributions, with painted goby having the narrowest salinity range and sand goby the widest. Moreover, data from paternity show that the two-spotted goby experiences the least sperm competition, whereas in the sand goby sperm competition is ubiquitous. The authors took sperm samples from dissected males and exposed them to high salinity water (31 PSU) representing the North Sea and low salinity water (6 PSU) representing the brackish Baltic Sea Proper. They then used computer-assisted sperm analysis to measure the proportion of motile sperm and sperm swimming speed 10 min and 20 h after sperm activation. The authors found that sperm performance depended on salinity, but there seemed to be no relationship to the species' geographical distribution in relation to salinity range. The species differed in the proportion of motile sperm, but there was no significant decrease in sperm motility during 20 h. The sand goby was the only species with motile sperm after 72 h.

Post-glacial establishment of locally adapted fish populations over a steep salinity gradient.

Studies of colonization of new habitats that appear from rapidly changing environments are interesting and highly relevant to our understanding of divergence and speciation. Here, we analyse phenotypic and genetic variation involved in the successful establishment of a marine fish (sand goby, Pomatoschistus minutus) over a steep salinity drop from 35 PSU in the North Sea (NE Atlantic) to two PSU in the inner parts of the post-glacial Baltic Sea. We first show that populations are adapted to local salinity in a key reproductive trait, the proportion of motile sperm. Thereafter, we show that genome variation at 22,190 single nucleotide polymorphisms (SNPs) shows strong differentiation among populations along the gradient. Sequences containing outlier SNPs and transcriptome sequences, mapped to a draft genome, reveal associations with genes with relevant functions for adaptation in this environment but without overall evidence of functional enrichment. The many contigs involved suggest polygenic differentiation. We trace the origin of this differentiation using demographic modelling and find the most likely scenario is that at least part of the genetic differentiation is older than the Baltic Sea and is a result of isolation of two lineages prior to the current contact over the North Sea-Baltic Sea transition zone.

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

During male-male competition, evolution can favor alternative reproductive tactics. This often results in a dominant morph that holds a resource, such as a nest for egg laying, which competes with a smaller sneaker morph that reproduces by stealing fertilizations. The salinity environment can influence male growth rates, for example, via osmoregulatory costs, which in turn may influence the use of sneaker tactics for small males competing for mating opportunities. Salinity can also affect sperm directly; however, little is known of how salinity influences sneaker tactics through sperm performance. We sampled males of the invasive round goby (Neogobius melanostomus) from two environments, a freshwater river and a brackish estuary. This fish has two male morphs: nest-holding dark males and non-nest-holding light males. We examined the role of water salinity of 0, 8, and 16 on sperm performance and found that for estuarine males, a salinity of 0 reduced sperm velocity compared to a salinity of 8 and 16. Riverine males had low velocity in all salinities. Sperm viability also decreased by over 30% in 0 salinity, compared to 8 and 16, for fish from both environments. Gobies produce ejaculate contents in specialized glands that could in theory shield sperm in an adverse environment. However, gland contents did not improve sperm performance in our tests. Body mass and age estimates indicate that riverine males invested more in somatic growth compared to estuarine males. Estuarine light morph males had a high enough gonadosomatic index to indicate sneaker tactics. We propose that when sperm performance is low, such as for the riverine males, sneaker tactics are ineffective and will be selected against or phenotypically suppressed. Instead, we interpret the increased investment in somatic growth found in riverine males as a life-history decision that is advantageous when defending a nest in the next reproductive season.

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

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.

Endless forms of sexual selection.

In recent years, the field of sexual selection has exploded, with advances in theoretical and empirical research complementing each other in exciting ways. This perspective piece is the product of a "stock-taking" workshop on sexual selection and sexual conflict. Our aim is to identify and deliberate on outstanding questions and to stimulate discussion rather than provide a comprehensive overview of the entire field. These questions are organized into four thematic sections we deem essential to the field. First we focus on the evolution of mate choice and mating systems. Variation in mate quality can generate both competition and choice in the opposite sex, with implications for the evolution of mating systems. Limitations on mate choice may dictate the importance of direct vs. indirect benefits in mating decisions and consequently, mating systems, especially with regard to polyandry. Second, we focus on how sender and receiver mechanisms shape signal design. Mediation of honest signal content likely depends on integration of temporally variable social and physiological costs that are challenging to measure. We view the neuroethology of sensory and cognitive receiver biases as the main key to signal form and the 'aesthetic sense' proposed by Darwin. Since a receiver bias is sufficient to both initiate and drive ornament or armament exaggeration, without a genetically correlated or even coevolving receiver, this may be the appropriate 'null model' of sexual selection. Thirdly, we focus on the genetic architecture of sexually selected traits. Despite advances in modern molecular techniques, the number and identity of genes underlying performance, display and secondary sexual traits remains largely unknown. In-depth investigations into the genetic basis of sexual dimorphism in the context of long-term field studies will reveal constraints and trajectories of sexually selected trait evolution. Finally, we focus on sexual selection and conflict as drivers of speciation. Population divergence and speciation are often influenced by an interplay between sexual and natural selection. The extent to which sexual selection promotes or counteracts population divergence may vary depending on the genetic architecture of traits as well as the covariance between mating competition and local adaptation. Additionally, post-copulatory processes, such as selection against heterospecific sperm, may influence the importance of sexual selection in speciation. We propose that efforts to resolve these four themes can catalyze conceptual progress in the field of sexual selection, and we offer potential avenues of research to advance this progress.

Pipefish embryo oxygenation, survival, and development: egg size, male size, and temperature effects.

In animals with uniparental care, the quality of care provided by one sex can deeply impact the reproductive success of both sexes. Studying variation in parental care quality within a species and which factors may affect it can, therefore, shed important light on patterns of mate choice and other reproductive decisions observed in nature. Using Syngnathus typhle, a pipefish species with extensive uniparental male care, with embryos developing inside a brood pouch during a lengthy pregnancy, we assessed how egg size (which correlates positively with female size), male size, and water temperature affect brooding traits that relate to male care quality, all measured on day 18, approximately 1/3, of the brooding period. We found that larger males brooded eggs at lower densities, and their embryos were heavier than those of small males independent of initial egg size. However, large males had lower embryo survival relative to small males. We found no effect of egg size or of paternal size on within-pouch oxygen levels, but oxygen levels were significantly higher in the bottom than the middle section of the pouch. Males that brooded at higher temperatures had lower pouch oxygen levels presumably because of higher embryo developmental rates, as more developed embryos consume more oxygen. Together, our results suggest that small and large males follow distinct paternal strategies: large males positively affect embryo size whereas small males favor embryo survival. As females prefer large mates, offspring size at independence may be more important to female fitness than offspring survival during development.

Understanding resource driven female-female competition: ovary and liver size in sand gobies.

The operational sex ratio (OSR, ready-to-mate males to females) is a key factor determining mating competition. A shortage of a resource essential for reproduction of one sex can affect OSR and lead to competition within the opposite sex for resource-holding mates. In the sand goby (Pomatoschistus minutus), a fish with paternal care, male readiness to mate depends on acquiring a nest-site, whereas food abundance primarily impacts female egg production. Comparing body condition and gonadal investment of fish from two populations with different availability in resources (Baltic Sea: few nest-sites, more food; North Sea: many nest-sites, less food), we predicted females carrying more mature eggs in the Baltic Sea than in the North Sea. As predicted, ovaries were larger in Baltic Sea females, and so was the liver (storage of energy reserves and vitellogenic compounds) for both sexes, but particularly for females. More females were judged (based on roundness scores) to be ready to spawn in the Baltic Sea. Together with a nest colonization experiment confirming a previously documented difference between the two areas in nest-site availability, these results indicate a more female-biased OSR in the Baltic Sea population, compared to the North Sea, and generates a prediction that female-female competition for mating opportunities is stronger in the Baltic population. To our knowledge, this is the first time that female reproductive investment is discussed in relation to OSR using field data.

Continuous but not intermittent noise has a negative impact on mating success in a marine fish with paternal care.

Anthropogenic underwater noise is a global pollutant of increasing concern but its impact on reproduction in fish is largely unknown. Hence, a better understanding of its consequences for this important link to fitness is crucial. Working in aquaria, we experimentally tested the impact of broadband noise exposure (added either continuously or intermittently), compared to a control, on the behaviour and reproductive success of the common goby (Pomatoschistus microps), a vocal fish with exclusive paternal care. Compared to the intermittent noise and control treatments, the continuous noise treatment increased latency to female nest inspection and spawning and decreased spawning probability. In contrast, many other female and male pre-spawning behaviours, and female ventilation rate (proxies for stress levels) did not differ among treatments. Therefore, it is likely that female spawning decisions were delayed by a reduced ability to assess male acoustic signals, rather than due to stress per se and that the silent periods in the intermittent noise treatment provided a respite where the females could assess the males. Taken together, we show that noise (of similar frequency range as anthropogenic boat noise) negatively affects reproductive success, particularly under a continuous noise exposure.

Sperm-duct gland content increases sperm velocity in the sand goby.

Sperm performance is often tightly linked to male reproductive success. In many demersal gobiid fishes, the male attaches sperm embedded in a mucus produced by sperm-duct glands to the nest substrate before spawning takes place. Sperm are activated as the mucus and embedded gland content dissolve into the water. To test the importance of gland content on sperm function in Pomatoschistus minutus, a marine fish with external fertilization, we used a paired experimental design, with spermatozoa tested with and without sperm-duct gland content mixed into seawater. We measured sperm velocity, percentage of motile sperm and sperm viability over time. Sperm were found to swim 7.3% faster when gland content was mixed in the seawater. Percentage motile sperm was unaffected by the gland content. Sperm viability in seawater exceeded 24 h, but was unaffected by the gland content. An increase in sperm velocity of similar magnitude as found here has been shown by others to increase fertilization success. Since velocity-boosting properties of sperm-duct gland content have now been found in three distantly related goby species, this trait appears to be conserved across the Gobiidae family and may aid in reproduction across a range of species and environments.This article has an associated First Person interview with the first author of the paper.

Why do some animals mate with one partner rather than many? A review of causes and consequences of monogamy.

Why do some animals mate with one partner rather than many? Here, I investigate factors related to (i) spatial constraints (habitat limitation, mate availability), (ii) time constraints (breeding synchrony, length of breeding season), (iii) need for parental care, and (iv) genetic compatibility, to see what support can be found in different taxa regarding the importance of these factors in explaining the occurrence of monogamy, whether shown by one sex (monogyny or monandry) or by both sexes (mutual monogamy). Focusing on reproductive rather than social monogamy whenever possible, I review the empirical literature for birds, mammals and fishes, with occasional examples from other taxa. Each of these factors can explain mating patterns in some taxa, but not in all. In general, there is mixed support for how well the factors listed above predict monogamy. The factor that shows greatest support across taxa is habitat limitation. By contrast, while a need for parental care might explain monogamy in freshwater fishes and birds, there is clear evidence that this is not the case in marine fishes and mammals. Hence, reproductive monogamy does not appear to have a single overriding explanation, but is more taxon specific. Genetic compatibility is a promising avenue for future work likely to improve our understanding of monogamy and other mating patterns. I also discuss eight important consequences of reproductive monogamy: (i) parentage, (ii) parental care, (iii) eusociality and altruism, (iv) infanticide, (v) effective population size, (vi) mate choice before mating, (vii) sexual selection, and (viii) sexual conflict. Of these, eusociality and infanticide have been subject to debate, briefly summarised herein. A common expectation is that monogamy leads to little sexual conflict and no or little sexual selection. However, as reviewed here, sexual selection can be substantial under mutual monogamy, and both sexes can be subject to such selection. Under long-term mutual monogamy, mate quality is obviously more important than mate numbers, which in turn affects the need for pre-mating mate choice. Overall, I conclude that, despite much research on genetic mating patterns, reproductive monogamy is still surprisingly poorly understood and further experimental and comparative work is needed. This review identifies several areas in need of more data and also proposes new hypotheses to test.