Abstract
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.
Highlights
Genetic adaptation and phenotypic plasticity (Chevin et al, 2010) facilitate the migration of organisms into new habitats and permit coping with changing environmental conditions (Brierley and Kingsford, 2009; Poloczanska et al, 2013; Urban, 2015)
Pipefish Adults From Low Saline Environment Have a Smaller Body Size Pipefish males and females caught in high origin salinity of the Baltic Sea were on average larger [mean ± standard deviation (SD), all high salinity sampling sites: 14.2 ± 2.1 cm; Flens: 14.4 ± 2.1 cm (n = 61), Falckensteiner Strand (Falck): 14.5 ± 2.0 cm (n = 59), Fehm: 13.8 ± 2.1 cm (n = 59)] than those from the low origin salinity [all low salinity sampling sites: 12.8 ± 2.0 cm; Salz: 14.0 ± 2.1 cm (n = 53), RuegN: 11.7 ± 1.6 cm (n = 48), RuegS: 12.4 ± 1.5 cm (n = 52): Figure 3A]
We found an interaction in the total length of adult pipefish between origin salinity and acclimation salinity [analysis of variance (ANOVA) F(1,320) = 7.4, p < 0.01; Supplementary Table 7A] indicating that parental acclimation salinity negatively affected growth of adult pipefish depending on the origin salinity
Summary
Genetic adaptation and phenotypic plasticity (Chevin et al, 2010) facilitate the migration of organisms into new habitats and permit coping with changing environmental conditions (Brierley and Kingsford, 2009; Poloczanska et al, 2013; Urban, 2015). Trans-generational plasticity (TGP) is the non-genetic inheritance of an alternative phenotype by transferring nutrients, hormones, proteins, or epigenetic marks from the parent to the offspring generation (Sunday et al, 2014). TGP can be adaptive and result in increased offspring performance when environmental conditions of parental and offspring generations match (Sunday et al, 2014). This has been shown for instance in wild Atlantic silversides exposed to ocean acidification (Murray et al, 2014) or in three-spined sticklebacks exposed to heat stress (Shama and Wegner, 2014). Mortality increased in the early life stages of sticklebacks upon changes in salinity levels of the parental generation (Heckwolf et al, 2018)
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