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

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 (Vibrio bacteria) stressor using six different populations of the broad-nosed pipefish Syngnathus typhle that 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 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 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.

Suboptimal environmental conditions prolong phage epidemics in bacterial populations

“…In times of environmental change, we predict that altered interactions and co‐evolutionary dynamics between phages and bacteria will also change higher order interactions, which are often mediated by phages (Wendling, 2023; Wendling et al, 2017). This can be further intensified when fast changes in abiotic parameters, such as salinity, require recourse allocation towards respective coping mechanisms, that is osmoregulation in host organisms, which impairs their immune systems and ultimately increases the impact of infections (Goehlich et al, 2021).…”

Are fish immunocompetent enough to face climate change?

“…Generally, the observed changes seem to be species, tissue and immune factor dependent. A few studies have indicated an acclimation and adaptation potential of fish immunity to salinity [132][133][134] ( possibly driven by genetic and epigenetic changes, see §4), hence chronic exposure studies are needed to study long-term salinity effects on disease susceptibility. Data in this area of ecoimmunology are still limited but by applying more standardized methods (see suggestions in §6) it may be possible to decipher general effects in future research.…”

Parent-specific transgenerational immune priming enhances offspring defense – unless heat-stress negates it all

“…Trans-generational plasticity provides an evolutionary opportunity for short-term acclimatization to changing environmental conditions by shaping the offspring phenotype through the transfer of parental experience (1)(2)(3)(4). Trans-generational plasticity can be adaptive and improve offspring survival in situations of rapid but predictable changes in abiotic conditions (e.g., temperature & salinity in marine habitats (5)(6)(7)(8)(9)(10)) as well as biotic conditions (e.g., changing microbial assemblage) in a matching parent-offspring environment (4,11,12). In the latter situation, trans-generational immune priming (TGIP; the transfer of parental immunological experience) was suggested to enhance offspring immune responses towards an infectious agent that parents have previously encountered.…”

“…A mismatch in the microbial assemblage between paternal and offspring environments, as well as a change of an additional abiotic environmental factor across generation, can induce costs of parentally-influenced constitutively upregulated immune responses in the offspring (48,49). While the latter may negatively influence offspring performance, TGIP that relies on inducible immune responses, might become ineffective when additional environmental factors change across generations, due to the resource-allocation trade-off involved (6,50,51). Disentangling constitutive from inducible influences of paternal immunological priming on offspring immune responses can thus illuminate how animals cope in a world of global change where emerging diseases can be a result of rapidly changing abiotic conditions.…”