Introduction
Ecological specialization, the spatial and temporal differentiation of species in the use of habitat and resources (Devictor et al.2010), is a pivotal eco-evolutionary paradigm to explain phylogeographical patterns, community assembly rules, and the majority of adaptive radiations (Gillespie et al. 2020; Mammola et al. 2020; Todd Streelman & Danley 2003; Wilson et al.2020). Despite the fact that marine fishes often show complex adaptations in spatially heterogeneous environments (e.g. Wainwright et al.2004; Wainwright et al.2015), ecological specialization is thought to be rare in marine species mainly because the geographic barriers in the vastness of seas are weak and planktonic larvae have the potential to maintain large population sizes with high gene flow (Palumbi 1994; Zhang et al.2016). Therefore, marine organisms challenge the classical theories of local adaptation and speciation, what has been dubbed the “Marine Speciation Paradox” (Bierne et al. 2003).
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). Although empirical examples of deep divergence in marine ecosystems are limited, molecular phylogenetic reconstructions of some marine fishes suggest that ecological specialization has a great impact on their diversification (e.g. Rocha et al. 2005; Wainwrightet al.2004). This is especially true for geographically widespread species that may experience considerably different ecological conditions across their distribution (Fox & Morrow 1981; Loxdale et al. 2011; Shipleyet al.2009). Divergent selection is an important element of natural selection, and occurs when different environments favor different phenotypes, leading to increased differences between populations (Bolnick & Stutz 2017). Theoretically, divergent selection should promote the evolution of traits in local populations that provide an advantage under local environmental conditions (Kawecki & Ebert 2004), and selection pressure may lead to genetic divergence and eventual speciation if the homogenizing effects of gene flow are insufficient to prevent it. In this regard, uncovering the differentiation among marine populations is of considerable importance for advancing our knowledge of the molecular mechanisms of adaptive evolution against a background of high-level gene flow.
The seaweed pipefish Syngnathus schlegeli (Kaup, 1856) is a well-known species in which there is exclusive paternal care of eggs (Watanabe & Watanabe 2001). The offsprings develop within the male brood pouch and are released as free-living juveniles. Syngnathus schlegeli is distributed along coastlines of the northwestern Pacific Ocean and generally inhabits sheltered areas in shallow waters; geographic range of this species encompasses a wide variety of climatic conditions and nearshore microhabitats (Chen et al. 2017; Zhang et al.2017). The vast region of the northwestern Pacific is characterized by distinct tectonic and geographical features, with a series of marginal seas separating the eastern Asian continent from the Pacific Ocean (Tamaki & Honza 1991). During the Pleistocene glacial cycles, the sea level fluctuations resulted in successive exposure and inundation of continental shelves, closure and opening of seaways, and separation and reunion of marginal seas (Wang 1999). When sea level falls, the seas were separated by land bridges extending between islands and the mainland, hindering the spread of most marine species (Ni et al.2014; Wang 1999). The historical influence of glaciation, which has been proposed as a dominant factor shaping present-day phylogeographical patterns (Hewitt 2004), distinguishes this area from other marine realms to such an extent that the glacial effects on its biota would be distinctly different from those revealed in other regions (Xu et al. 2009).
In this study, we investigated the cranial morphology, genetic structure, and ecological niche of S. schlegeli along China seashores to reveal the phylogeographical patterns resulting from adaptive radiation and ecological specialization. Firstly, we used geometric morphometrics to partition the variations in the cranial morphology among populations. Secondly, we employed the restriction-site-associated DNA sequencing (RADseq) technique to evaluate the level of genetic differentiation among seaweed pipefish populations based on the genome-wide genotypic and sequence data. Finally, we compared the ecological niches of independent S. schlegeli populations using n –dimensional hypervolumes, and mapped habitat suitability of this species during present–day and the Last Glacial Maximum (LGM) using species distribution model (SDM). By revisiting the phylogeographical history of the widespread pipefish using an integrative approach, our over-arching goal is to investigate the dynamics through which local specialization could arise in the apparent absence of dispersal barriers.