The evolution of ecological specialization across the range of a broadly distributed marine species

Abstract

Ecological specialization is an important engine of evolutionary change and adaptive radiation, but empirical evidence of local adaptation in marine environments is rare, a pattern that has been attributed to the high dispersal ability of marine taxa and limited geographic barriers to gene flow. The broad‐nosed pipefish, Syngnathus typhle, is one of the most broadly distributed syngnathid species and shows pronounced variation in cranial morphology across its range, a factor that may contribute to its success in colonizing new environments. We quantified variation in cranial morphology across the species range using geometric morphometrics, and tested for evidence of trophic specialization by comparing individual‐level dietary composition with the community of prey available at each site. Although the diets of juvenile pipefish from each site were qualitatively similar, ontogenetic shifts in dietary composition resulted in adult populations with distinctive diets consistent with their divergent cranial morphology. Morphological differences found in nature are maintained under common garden conditions, indicating that trophic specialization in S. typhle is a heritable trait subject to selection. Our data highlight the potential for ecological specialization in response to spatially variable selection pressures in broadly distributed marine species.

Revisiting the ‘Marine Speciation Paradox’ using genomic, morphometric, and ecological evidence in pipefish

“…A similar phylogeographical pattern have been documented in the northwestern Pacific using fishes, molluscs, and crustaceans (Liu et al 2007;Ni et al 2012;Wilsonet al 2020;Xu et al 2009). In marine environments, worldwide glaciation is confirmed to be the most efficient way in generating intraspecific genetic splits (Hewitt 2000), as well as shaping the present-day phylogeographical pattern of marine species (Dong et al 2012;Wilson et al 2020). Example of this have been found in different biogeographic realms, from the Indo-West Pacific to the Atlantic and Mediterranean basins (Cunhaet al 2008;Ni et al 2014).…”

“…schlegeli from different geographic regions diverge in their realized niche, implying that the three clades have adapted to largely distinct environmental conditions including temperature and salinity. A recent study of Syngnathus typhle based on geometric morphometrics, prey availability, and dietary composition, demonstrated a pronounced variation in snout morphology across its distribution range, which may contribute to its adaptation in novel environments (Wilson et al 2020). In the present study, a north-to-south variation of cranial morphology was detected in different S. schlegeli populations, which indicates that the individuals in the south of the distributional range (SCS) have smaller eye, and the opposite patterns are observed in the north (ECS and YS).…”

Exploring ecological specialization in pipefish using genomic, morphometric and ecological evidence

“…The ecological processes, along with local adaptation, are most important responses of species to the changing environment, which both contribute to the specialization. Several recent studies on marine species have demonstrated population differentiation consistent with local adaptation and trophic partitioning in spatially heterogeneous environments (Rocha et al, 2005;Sanford & Kelly, 2011;Sanford & Worth, 2010;Wilson et al, 2020). In this regard, uncovering the differentiation among marine populations is of considerable importance for advancing our knowledge on the molecular mechanisms of adaptive evolution against a background of high-level gene flow.…”

“…The importance of natural selection in shaping adaptive trait differentiation among natural populations has long been recognized (Garant et al, 2005;Smith et al, 1997). Theory predicts that once populations are exposed to diverse ecological environments, rapid evolution of adaptive traits should occur (Hendry et al, 2000), and phylogeographical structuring along ecological gradients has been documented in many marine species (Liu et al, 2007;Ni et al, 2012;Wilson et al, 2020;Xu et al, 2009). Divergent selection is an important element of natural selection and occurs when different environments favour different phenotypes, leading to increased differences between populations (Bolnick & Stutz, 2017).…”

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

“…A suitable organism to study the interactive contribution of genetic adaptation and phenotypic plasticity is the broad-nosed pipefish Syngnathus typhle (Syngnathidae, Teleostei) (Wilson et al, 2020). S. typhle inhabits a wide range of waters with different salinity levels along the European coastline from the Black Sea in Eastern Europe to the Mediterranean Sea and the Eastern Atlantic (Wilson and Veraguth, 2010).…”