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.