Strong genetic structure in a widespread estuarine crab: A test of potential versus realized dispersal

Abstract

Aim: Genetic structure has proven difficult to predict for marine and estuarine species with multi-day pelagic larval durations, since many disperse far less than expected based on passive transport models. In such cases, the gap between potential and realized dispersal may result from larval behaviours that evolved to facilitate retention and settlement in favourable environments. Behaviour is predicted to play a particularly key role in structuring truly estuarine species, which often moderate their behaviour to remain within their natal estuaries. In such systems, this restricted dispersal may lead to high divergence, local adaptation and eventual speciation across their range. Here, we test whether a geographically widespread estuarine crab, known to have behaviour promoting larval retention, exhibits high population structure despite a 2-to 4-week larval duration. Location: Atlantic and Gulf Coasts of North America. Taxon: White-fingered mud crab, Rhithropanopeus harrisii. Methods: Population genomic analyses across nine estuaries from New Hampshire to Louisiana using 12,638 transcriptome-derived SNPs. Results: We found highly differentiated genetic signatures among all nine estuaries, separated by 200-5,000 km of coastline. Estimates of gene flow suggest that migration is low and largely symmetrical between sites. We also observed deep phylogenetic divides corresponding to major biogeographical breaks. Main conclusions: These results indicate substantial and longstanding constraints to dispersal in the species' native range, likely arising from the emergence of geological and oceanographic barriers and sustained by behaviour that promotes estuarine retention during larval development. This work supports the idea that larval behaviour promoting estuarine retention can be reflected in substantial genetic structure even in species with multi-week pelagic larval durations. Such behaviour-restricted dispersal has implications for predicting adaptation and spread in estuarine species, many of which have been introduced outside their native ranges.

Invasion history shapes host transcriptomic response to a body‐snatching parasite

“…Sequence data from these specimens were generated previously, as described in Tepolt, Blakeslee, et al (2020). As the largest and most accessible neural organ, the thoracic ganglion was chosen for sequencing due to its probable functional importance to the parasite's impact on host behaviour.…”

“…Libraries were sequenced across seven lanes of an Illumina HiSeq 2000 in 50‐bp single‐end reads at the University of Utah High Throughput Genomics Core Facility. Further methodological details, including the results of a population genomic investigation of the host crab, can be found in Tepolt, Blakeslee, et al (2020).…”

“…To identify potential contamination from reads originating from the parasite, sequences were aligned to a Loxothylacus panopaei transcriptome that had been previously assembled from sequencing of two parasite externae, one each from the parasite's native (LA) and invasive (MD) ranges. The parasite transcriptome was assembled as per Tepolt, Blakeslee, et al (2020) and reads from host libraries were screened against it using magic‐blast (Boratyn et al, 2019); reads aligning across their entire length with ≥98% identity were removed using bbtools (https://sourceforge.net/projects/bbmap).…”

Population structure and phylogeography of two North Atlantic Littorina species with contrasting larval development

“…Even so, the contrasting patterns of observed genetic diversity in our study reflect variation in just a single mitochondrial marker. Future studies with more nuclear markers could resolve this issue (e.g., population genome sequencing; Reitzel et al 2013;Tepolt et al 2020). Indeed, L. saxatilis has recently become the subject of numerous genomic investigations of ecotypic differentiation across multiple European populations (e.g., Johannesson et al 2017Johannesson et al , 2020Kess et al 2018;Morales et al 2019), approaches that could be applied to North American populations to further resolve its population structure throughout the North Atlantic.…”

“…In fact, some studies have found pelagically dispersing species to exhibit relatively high levels of genetic structure than might otherwise be expected considering their larval duration (Milá et al 2017;Mertens et al 2018). For example, the white-fingered mud crab, Rhithropanopeus harrisii, has a planktotrophic larval stage and demonstrates strong genetic structure in Gulf and Atlantic estuaries in its North American range, with larval retention behaviors likely playing a role (Tepolt et al 2020). Second, genetic variability could be lower than expected for marine taxa with pelagically dispersing larvae if there is high larval mortality during the pelagic stage (i.e., type III survivorship curves) (Hedgecock 1994).…”