Crawling to connectivity? The direct-developing journey of the spotted whelk (Cominella maculosa)

Abstract

<p>The exchange of individuals between populations influences demographic connectivity on the ecological scale and genetic connectivity on the evolutionary scale. In some circumstances there are similarities between demographic and genetic connectivity, but in others there are differences. Whenever genetic differentiation is found between populations demographic uncoupling can also be inferred, but when gene flow is found there is uncertainty about whether populations are demographically connected or not. Marine invertebrates typically have large population sizes and many opportunities for dispersal. However, species that have limited planktonic dispersal power are often characterized by genetically and demographically discrete populations that exhibit an isolation-by-distance (IBD) pattern of gene distribution. Alternative methods of dispersal, such as rafting or drifting, produce departures from this expected pattern for species lacking planktonic larvae. Examining genetic patterns at fine geographic scales can identify key dispersal barriers and may give clues to alternative dispersal methods influencing large scale processes. The endemic, direct-developing spotted whelk, Cominella maculosa, is found in the intertidal rocky shores throughout most of New Zealand. This distribution makes it ideal for studying a species expected to exhibit low realized dispersal by crawling and is unlikely to experience dispersal by rafting. The first aim of this study was to investigate genetic patterns between two genetically distinct populations along the Wairarapa Coast of the North Island to determine if a barrier to dispersal was present or if the expected IBD pattern was observed. The second aim was to determine the likelihood of individual hatchlings undertaking long distance dispersal by drifting in the water column. The mitochondrial DNA COI gene was sequenced using 324 whelk samples collected at seven sites along 125 km of Wairarapa shoreline. No significant level of genetic isolation-by-distance or discontinuity in haplotype distribution was observed. Instead, two sites in the middle of the region form a contact area where the dominant northern and southern haplotypes coexist. To investigate dispersal by drifting in the water, three experimental trials were conducted with hatchlings obtained from field-collected egg capsules. When subjected to wave forces, or deposited directly in flow, hatchlings remained suspended and were carried a short distance. However, hatchlings circulated in currents and left for a longer period (12 hours) were rarely found drifting after this period. These trials indicate that wave dislodgement and local flow regime may result in small-scale displacement of hatchlings, but long-distance dispersal by drift is unlikely. Plankton sampling was also conducted at two sites with four nearshore traps. The rare capture of a related Cominella virgata hatchling supports the finding that hatchlings can be dislodged, but prolonged drift cannot be inferred. The findings from this study support the assumption that crawling is the dominant dispersal mechanism for C. maculosa. Crawling between sites best explains the blending of haplotypes in the middle of the Wairarapa and the genetic differentiation between populations. Crawling-mediated connectivity is unlikely to occur at the ecological scale; therefore populations are expected to be demographically isolated. The results of this research support the general findings in the literature that populations of direct developing species are often demographically isolated and have low levels of genetic connectivity.</p>

The Phylogeography and Demographic History of the Direct-Developing Coastal Gastropod Haustrum haustorium

“…haustorium's haplotype diversity is relatively high compared to its nucleotide diversity which suggests a population expansion (Grant and Bowen, 1998) due to the accumulation of mutations during the expansion (Figure 3.6). This is similar to the haplotype diversity and nucleotide diversity of C. virgata and C. maculosa, both of which show evidence of having undergone a population expansion (Dohner, 2016., Walton, 2017. H. scobina sensu lato have a high haplotype diversity paired relatively high nucleotide diversity.…”

“…(Tan, 2003), but it is possible that these egg capsules could be dislodged from the substrata and drift. Dohner (2016) found that the egg capsules of another gastropod species Cominella maculosa could be detached from the substrata and drift in the water column. Laboratory experiments found that egg capsules belonging to C. maculosa could drift in the water column and be carried short distances by the currents, though evidence for long-distance drifting is lacking.…”

“…Laboratory experiments found that egg capsules belonging to C. maculosa could drift in the water column and be carried short distances by the currents, though evidence for long-distance drifting is lacking. Dohner (2016) concludes that this egg drifting capability could allow for small-scale dispersal but is insufficient to fuel population connectivity on a geographic scale. Whether H. haustorium egg capsules have this capability is unknown, but the similarities shared by both C. maculosa and H. haustorium regarding egg laying means that egg capsule drift is not impossible.…”

“…All raw sequence chromatograms were edited by eye for insertions, deletions, and unresolved nucleotides within Geneious Prime 2022.1.1. COI sequences were trimmed to 610 bp in Geneious Prime to make them consistent with similar studies of coastal gastropods (Dohner, 2016., Walton, 2017., Fleming et al, 2018., Logan, 2019., O'Mahony, 2021. Nucleotide compositions, number of singleton, segregating, and parsimony-informative sites were obtained in MEGA11 (Tamura et al, 2021).…”

“…Ultimately, it is not clear what whether there was an unusual mode of migration that enabled haplotype 7 to become so prevalent at Castlepoint. Human-mediated translocation events are hypothesized to have occurred in similar New Zealand gastropod species like in the Cominella genus (Dohner, 2016., Walton, 2017., Fleming et al, 2018, and serve as a possible explanation for why some haplotypes occur in geographic locations that they are not expected to be found at. Outside of New Zealand, human-mediated translocation of coastal fauna is not uncommon.…”