Pipefish Locally Adapted to Low Salinity in the Baltic Sea Retain Phenotypic Plasticity to Cope With Ancestral Salinity Levels

Genetic adaptation and phenotypic plasticity facilitate the migration into new habitats and enable organisms to cope with a rapidly changing environment. In contrast to genetic adaptation that spans multiple generations as an evolutionary process, phenotypic plasticity allows acclimation within the life-time of an organism. Genetic adaptation and phenotypic plasticity are usually studied in isolation, however, only by including their interactive impact, we can understand acclimation and adaptation in nature. We aimed to explore the contribution of adaptation and plasticity in coping with an abiotic (salinity) and a biotic (Vibriobacteria) stressor using six different populations of the broad-nosed pipefishSyngnathus typhlethat originated from either high [14–17 Practical Salinity Unit (PSU)] or low (7–11 PSU) saline environments along the German coastline of the Baltic Sea. We exposed wild caught animals, to either high (15 PSU) or low (7 PSU) salinity, representing native and novel salinity conditions and allowed animals to mate. After male pregnancy, offspring was split and each half was exposed to one of the two salinities and infected withVibrio alginolyticusbacteria that were evolved at either of the two salinities in a fully reciprocal design. We investigated life-history traits of fathers and expression of 47 target genes in mothers and offspring. Pregnant males originating from high salinity exposed to low salinity were highly susceptible to opportunistic fungi infections resulting in decreased offspring size and number. In contrast, no signs of fungal infection were identified in fathers originating from low saline conditions suggesting that genetic adaptation has the potential to overcome the challenges encountered at low salinity. Offspring from parents with low saline origin survived better at low salinity suggesting genetic adaptation to low salinity. In addition, gene expression analyses of juveniles indicated patterns of local adaptation,trans-generational plasticity and developmental plasticity. In conclusion, our study suggests that pipefish are locally adapted to the low salinity in their environment, however, they are retaining phenotypic plasticity, which allows them to also cope with ancestral salinity levels and prevailing pathogens.

Evolutionary dynamics of the OR gene repertoire in teleost fishes: evidence of an association with changes in olfactory epithelium shape

Teleost fishes perceive their environment through a range of sensory modalities, among which olfaction often plays an important role. Richness of the olfactory repertoire depends on the diversity of receptors coded by homologous genes classified into four families: OR, TAAR, VR1 and VR2. Herein, we focus on the OR gene repertoire. While independent large contractions of the OR gene repertoire associated with ecological transitions have been found in mammals, little is known about the diversity of the OR gene repertoire and its evolution within teleost fishes, a group that includes more than 34,000 living species. We analyzed genomes of 163 species representing diversity in this large group. We found a large range of variation in the number of functional OR genes, from 15 in Syngnathus typhle and Mola mola, to 429 in Mastacembelus armatus. The number of OR genes was higher in species with an extensively folded olfactory epithelium, that is, for example, when a multi-lamellar rosette was present in the olfactory organ. Moreover, the number of lamellae was correlated with the richness of the OR gene repertoire. While a slow and balanced birth-and-death process generally drives evolution of the OR gene repertoire, we inferred several episodes of high rates of gene loss, sometimes followed by large gains in the number of OR genes. These gains coincide with morphological changes of the olfactory organ and suggest a strong functional association between changes in the morphology and the evolution of the OR gene repertoire.

Pipefish locally adapted to low salinity in the Baltic Sea retain phenotypic plasticity to cope with ancestral salinity levels

Genetic adaptation and phenotypic plasticity facilitate the invasion of new habitats and enable organisms to cope with a rapidly changing environment. In contrast to genetic adaptation that spans multiple generations as an evolutionary process, phenotypic plasticity allows acclimation within the life-time of an organism. Genetic adaptation and phenotypic plasticity are usually studied in isolation, however, only by including their interactive impact, we can understand acclimation and adaptation in nature. We aimed to explore the contribution of adaptation and plasticity in coping with an abiotic (salinity) and a biotic (Vibrio bacteria) stressor using six different populations of the broad-nosed pipefish Syngnathus typhle that originated from either high or low saline environments. We hypothesized that wild S. typhle populations are locally adapted to the salinity and prevailing pathogens of their native environment, and that short-term acclimation of parents to a novel salinity may aid in buffering offspring phenotypes in a matching environment. To test these hypotheses, we exposed all wild caught animals, to either high or low salinity, representing native and novel salinity conditions and allowed animals to mate. After male pregnancy, offspring was split and each half was exposed to one of the two salinities and infected with Vibrio alginolyticus bacteria that were evolved at either of the two salinities in a fully reciprocal design. We investigated life history traits of fathers (offspring survival, offspring size) and expression of 47 target genes in mothers and offspring.Pregnant males originating from high salinity exposed to low salinity were highly susceptible to opportunistic fungi infections resulting in decreased offspring size and number. In contrast, no signs of fungal infection were identified in fathers originating from low saline conditions suggesting that genetic adaptation has the potential to overcome the challenging conditions of low salinity. Genetic adaptation increased survival rates of juveniles from parents in lower salinity (in contrast to those from high salinity). Juvenile gene expression indicated patterns of local adaptation, trans-generational plasticity and developmental plasticity. The results of our study suggest that pipefish locally adapted to low salinity retain phenotypic plasticity, which allows them to also cope with ancestral salinity levels and prevailing pathogens.

Feeding ecology of pipefish species inhabiting Mediterranean seagrasses

Pipefish are a vulnerable and diverse group of ichthyofauna tightly associated to seagrass meadows, key habitats in shallow marine areas. Despite of their charismatic role, main ecological features, habitat and diet of this group remain largely unknown. This study focuses on assessing pipefish habitat and feeding preferences including different hosting seagrasses such as Posidonia oceanica and Cymodocea nodosa from the Balearic Islands, western Mediterranean. Four species (Syngnathus typhle, S. abaster, Nerophis ophidion and N. maculatus) were found associated to different seagrasses. S. typhle and N. maculatus were more frequent in P. oceanica meadows, while S. abaster and N. ophidion in C. nodosa. Individuals of all species captured in P. oceanica were larger than those living in C. nodosa, suggesting a size-dependent habitat preference. Feeding preferences, however, were driven by prey availability and fish features, e.g head/snout morphology. For the first time in the western Mediterranean, a thorough description of the diet and potential preys of this group was carried out. Epifaunal assemblages (potential prey) were dominated in both habitats by harpacticoid copepods and gammarid amphipods, and they were also the primary preys according to stomach contents of all species. These results can contribute to future pipefish conservation and management actions, such as targeting crucial habitat identification and designing culture and reintroduction protocols.

Parental investment and immune dynamics in sex-role reversed pipefishes

Parental care elevates reproductive success by allocating resources into the upbringing of the offspring. However, it also imposes strong costs for the care giving parent and can foster sexual dimorphism. Trade-offs between the reproductive system and the immune system may result in differential immunological capacities between the care-providing and the non-care-providing parent. Usually, providing care is restricted to the female sex making it impossible to study a sex-independent influence of parental investment on sexual immune dimorphism. The decoupling of sex-dependent parental investment and their influences on the parental immunological capacity, however, is possible in syngnathids, which evolved the unique male pregnancy on a gradient ranging from a simple carrying of eggs on the trunk (Nerophinae, low paternal investment) to full internal pregnancy (Syngnathus, high paternal investment). In this study, we compared candidate gene expression between females and males of different gravity stages in three species of syngnathids (Syngnathus typhle, Syngnathus rostellatus and Nerophis ophidion) with different male pregnancy intensities to determine how parental investment influences sexual immune dimorphism. While our data failed to detect sexual immune dimorphism in the subset of candidate genes assessed, we show a parental care specific resource-allocation trade-off between investment into pregnancy and immune defense when parental care is provided.

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.