Cryptic lineages, cryptic barriers: historical seascapes and oceanic fronts drive genetic diversity in supralittoral rockpool beetles (Coleoptera: Hydraenidae)

Abstract

Morphologically cryptic lineages confound many estimates of global biodiversity and are often discovered in ecologically specialized taxa, subject to strong morphological constraint. Such a situation may apply in many extreme environments, including supralittoral rockpools, where dramatic fluctuations in water availability and salinity impose strong selection pressures on the inhabitants. Here we explore the genetic diversity and phylogeography of supralittoral rockpool Ochthebius beetles in the eastern Atlantic and western Mediterranean, using a combination of mitochondrial and nuclear markers and dense geographical sampling of the three recognized widespread species. Our results point to the existence of morphologically cryptic lineages within all currently named taxa and suggest that the distribution of these is linked to both historical and contemporary marine hydrogeography; a combination of ocean currents and winds apparently driving the spatial patterns observed. The main contemporary barrier to dispersal for Ochthebius is located around the Ibiza Channel, whilst the Messinian Salinity Crisis appears to have been the ultimate driver of lineage diversification in these insects. Our results show that oceanographic processes do not just shape the evolution of fully marine species, but also impact significantly on the terrestrially derived inhabitants of the coastal zone.

Flight Dispersal in Supratidal Rockpool Beetles

“…The absence of a detectable influence of distance may be attributed to either a recent range expansion or a notable homogenising effect of gene flow related to dispersal [ 29 ]. Notably, a recent expansion into the Mediterranean has been previously suggested for O. lejolisii , a species initially considered restricted to the Atlantic Sea [ 39 ]. At a larger spatial scale (hundreds of km), Villastrigo et al [ 38 ], using other molecular markers (COI and wingless), found a lack of significant relationships between genetic and geographical distance, suggesting that additional factors played a more important role in the genetic structure of Ochthebius populations, such as oceanic currents.…”

“…Coastal Ochthebius may passively disperse via the transport of eggs by endo- and epizoochory with seabirds that frequently occur in rockpools, although no cases of phoresy have been documented in these species [ 38 ]. However, passive dispersal through marine currents may be the main method by which these insects disperse as marine plankton over medium to large spatial scales [ 38 , 39 , 40 ]. Therefore, the population genetic structure of the two Ochthebius species was predicted from the general circulation pattern of Mediterranean marine currents and associated oceanic fronts [ 38 ].…”

Novel Microsatellite Loci, Cross-Species Validation of Multiplex Assays, and By-Catch Mitochondrial Genomes on Ochthebius Beetles from Supratidal Rockpools

“…These adverse conditions are so challenging that only adapted species can thrive there [34,35]. In this context, the very small (1-2 mm) aquatic beetles of the worldwide distributed genus Ochthebius Leach, 1815 (Coleoptera: Hydraenidae) are capable of inhabiting these extreme environments, with some of them exhibiting cryptic diversity [36] and even partial sympatry with overlapping niches [16]. However, Ochthebius species are absent in the intertidal zone, where the area is regularly covered by water with periods of circadian, circatidal, or circalunadian rhythms, and its organisms have a series of adaptations to it (in addition to physiological ones, they can also present avoidance mechanisms, fixation structures, and mechanical resistance) [37,38].…”

“…Mapping distribution ranges and population boundaries in insects is a difficult task [39,40], particularly within cryptic species groups like the mentioned Mediterranean supralittoral species of the genus Ochthebius [35,36,[41][42][43]. In addition, many of these habitats face serious threats due to land use changes, such as coastal development [44], resulting in fragmentation and/or habitat loss that negatively impacts population connectivity and viability.…”

“…In addition, many of these habitats face serious threats due to land use changes, such as coastal development [44], resulting in fragmentation and/or habitat loss that negatively impacts population connectivity and viability. Recent studies have used a combination of mitochondrial and nuclear markers to identify morphologically cryptic lineages within recognized taxa in the eastern Atlantic and western Mediterranean [36,42]. However, achieving finer resolution is essential to validate potential lineages and to fully understand their connectivity patterns among populations [40].…”