Genomic Divergence in Stichopus cf. horrens
Sympatric Lineages
The sea cucumber Stichopus cf. horrens is a widespread and commercially important species found across the Indo-Pacific region. However, recent genetic studies have uncovered a surprising degree of cryptic diversity within this nominal taxon. Using a combination of mitochondrial DNA sequencing and nuclear microsatellite markers, researchers have identified at least three genetically distinct lineages or “species” that co-occur in sympatry across parts of the species’ range.
Genetic Diversity
Analysis of the mitochondrial cytochrome oxidase I (COI) gene revealed two highly divergent clades (Clade A and Clade B) within the Stichopus cf. horrens complex. These two clades are estimated to have diverged approximately 1.35-2.54 million years ago, suggesting they represent reproductively isolated evolutionary lineages. Interestingly, while Clade A haplotypes were more geographically widespread and abundant, Clade B contained an additional putative cryptic species-level subdivision (Clade B1 and Clade B2) that further warrants investigation.
Multilocus microsatellite genotyping provided independent nuclear genomic evidence supporting the mitochondrial lineages. Two genetically distinct microsatellite clusters (Cluster 1 and Cluster 2) were identified, with the majority of Clade A individuals sorting into Cluster 1 and Clade B individuals into Cluster 2. A small proportion of individuals exhibited admixed ancestry, suggesting limited contemporary gene flow between the two clusters.
Phylogenetic Relationships
Phylogenetic analyses of the COI data placed the Stichopus cf. horrens lineages alongside the closely related species S. horrens and S. monotuberculatus. While these latter two species did not form monophyletic groups, the majority of S. monotuberculatus sequences clustered within Clade A, while most S. horrens sequences were found in Clade B. This underscores the taxonomic uncertainty surrounding the delineation of these morphologically similar sea cucumber species.
The genetic divergence observed between Clade A and Clade B of Stichopus cf. horrens (2.79% for COI) is comparable to levels typically used to define distinct species in other echinoderms. The additional putative cryptic lineage within Clade B (B1 and B2) also exhibited significant genetic differentiation, suggesting the potential for further undescribed diversity within this complex.
Ecological Factors
Habitat Preferences
The sympatric Stichopus cf. horrens lineages appear to occupy similar shallow reef and soft-bottom habitats across the western Pacific. However, subtle differences in their geographic distributions and relative abundances suggest potential niche partitioning or adaptation to local environmental conditions.
Clade A haplotypes were more widespread and abundant, occurring at all sampled sites, while Clade B was less common and detected at only 10 of the 16 sites surveyed. Within Clade B, the B1 and B2 subgroups exhibited a degree of geographic structuring, with B1 predominantly in the eastern regions and B2 in the western regions.
Environmental Influences
The divergence and persistence of these sympatric lineages in the face of potential homogenizing gene flow likely involves a combination of prezygotic and postzygotic reproductive barriers. Factors such as differences in spawning timing, gamete incompatibilities, or selection against hybrids may all play a role in maintaining species boundaries.
Environmental heterogeneity across the species’ range, including differences in temperature, currents, and productivity, could also contribute to adaptive divergence and the evolution of reproductive isolation. Further research is needed to elucidate the specific ecological and evolutionary mechanisms driving lineage diversification within Stichopus cf. horrens.
Evolutionary Processes
Speciation Events
The deep divergence between the two major Stichopus cf. horrens clades (Clade A and Clade B) likely reflects a relatively ancient speciation event, possibly driven by vicariance or other isolating mechanisms in the past. The additional subdivision within Clade B (B1 and B2) may represent a more recent speciation process, potentially facilitated by adaptive divergence and the maintenance of reproductive barriers in sympatry.
The co-occurrence of these genetically distinct lineages, with limited evidence of contemporary hybridization, suggests that speciation in broadcast spawning marine invertebrates like sea cucumbers can occur even in the absence of obvious geographic barriers to gene flow. Mechanisms such as gamete recognition, spawning asynchrony, or postzygotic incompatibilities may play crucial roles in driving and maintaining species boundaries.
Adaptation Mechanisms
The identification of highly divergent genomic regions between the Stichopus cf. horrens lineages, including loci associated with rhodopsin and tachykinin receptor signaling, sperm motility, and hormone response, provides intriguing insights into the potential adaptive mechanisms underlying their divergence.
These genomic regions may be involved in prezygotic reproductive barriers, such as differences in spawning cues, gamete recognition, or sperm-egg interactions. Postzygotic incompatibilities, mediated by genetic incompatibilities or differences in physiological tolerance, could also contribute to the maintenance of species boundaries. Further investigation of the functional significance of these divergent genomic regions is warranted to better understand the evolutionary processes shaping this species complex.
Biogeographic Patterns
Geographic Distribution
The widespread distribution of the Stichopus cf. horrens species complex across the western Pacific, from the South China Sea to the central and eastern Pacific, suggests a long evolutionary history in the region. The relative abundance and geographic structuring of the major mitochondrial clades (Clade A and Clade B) and subclades (B1 and B2) hint at complex biogeographic patterns that may be influenced by historical vicariance events, ocean circulation patterns, and other environmental factors.
The apparent overlap in the geographic ranges of the sympatric lineages, with limited evidence of spatial segregation, underscores the importance of integrating genetic data with ecological and morphological information to fully resolve species boundaries and distribution patterns within this group.
Range Expansion
The potential for range expansion and invasion by sea cucumbers, including Stichopus cf. horrens, is a growing concern, particularly given the commercial importance and overfishing pressures on many holothurian species. Understanding the genetic diversity and evolutionary dynamics within this species complex can inform conservation and management strategies, as well as help predict the potential for range shifts or the introduction of non-native lineages.
Further research, including the development of robust genetic markers and the assessment of connectivity patterns across the species’ range, will be crucial for monitoring and managing Stichopus cf. horrens populations in the face of ongoing environmental change and human impacts. Such insights can also inform the broader understanding of speciation processes and biodiversity in tropical marine ecosystems.
In conclusion, the genomic divergence and cryptic diversity uncovered within the Stichopus cf. horrens species complex highlight the importance of integrating multiple lines of evidence, including molecular, ecological, and morphological data, to fully resolve the taxonomy and evolutionary history of this commercially and ecologically important group of sea cucumbers. These findings have significant implications for the management and conservation of holothurian resources across the Indo-Pacific region.
