Species-specific genetic variation in response to deep-sea environmental variation amongst Vulnerable Marine Ecosystem indicator taxa

Abstract

Understanding the ecological processes that shape spatial genetic patterns of population structure is critical for understanding evolutionary dynamics and defining significant evolutionary and management units in the deep sea. Here, the role of environmental factors (topographic, physico-chemical and biological) in shaping the population genetic structure of four deep-sea habitat-forming species (one sponge -Poecillastra laminaris, three corals -Goniocorella dumosa, Madrepora oculata, Solenosmilia variabilis) was investigated using seascape genetics. Genetic data (nuclear and mitochondrial sequences and microsatellite multilocus genotypes) and environmental variables were employed to build individual-based and population-level models. The results indicated that environmental factors affected genetic variation differently amongst the species, as well as at different geographic scales. For individual-based analyses, different environmental variables explained genetic variation in P. laminaris (dissolved oxygen), G. dumosa (dynamic topography), M. oculata (sea surface temperature and surface water primary productivity), and S. variabilis (tidal current speed). At the population level, factors related to current and food source explained the regional genetic structure in all four species, whilst at the geomorphic features level, factors related to food source and topography were most important. Environmental variation in these parameters may be acting as barriers to gene flow at different scales. This study highlights the utility of seascape genetic studies to better understand the processes shaping the genetic structure of organisms, and to identify environmental factors that can be used to locate sites for the protection of deep-sea Vulnerable Marine Ecosystems.How spatially variable environmental and habitat features influence evolutionary processes and population genetic connectivity in the deep sea is poorly understood 1-3 . The deep-sea environment experiences increasing pressure, decreasing pH, and generally decreasing temperature, with increasing depth 4 . Such single factor or multi-factorial gradients may strongly influence dispersal, settlement and recruitment patterns of deep-sea taxa 5-7 . Additionally, features such as bottom currents 8 , surface currents 9 and bathymetry may play important roles in shaping the patterns of genetic connectivity amongst populations in many deep-sea species 5,10,11 , with the result that multiple environmental factors may act as barriers to or promoters of gene flow in the deep sea 8,9,12 and thereby strongly influence population genetic structure at different spatial and even temporal scales. However, the complexity of the deep-sea physico-chemical environment and the logistical difficulties of sampling (both biological specimens and environmental data) such a large biome have limited our ability to understand multispecies patterns of population genetic structure and how these are influenced by environmental variation 3,13-15 .Deep-sea vulnerable marine ecosystems (VMEs) ...

Macroecological trend of increasing values of intraspecific genetic diversity and population structure from temperate to tropical streams

“…The discordance found in estimates of population structure across co‐distributed species indicates the importance of both lineage‐specific functional traits and local demographic fluctuations in driving large‐scale patterns of intraspecific genetic variation. In fact, a pattern based on dispersal propensity is apparent here, revealing how environmental factors had different effects on the genetic variation of co‐distributed species that differ in functional traits (Zeng et al., 2020). The mayflies, which show weak dispersal propensity, presumably attributable to their short adult life span, did generally show higher estimates of Φ ST than the highly dispersive co‐distributed beetles.…”

Rapid deep ocean deoxygenation and acidification threaten life on Northeast Pacific seamounts

“…TA B L E 2 Each indicator taxon, the zone it belongs to, its common and scientific name, number of individuals observed in the 2017 visual surveys, the mean (µ) and standard deviation (σ) of its depth range (2017), its vertical distribution-weighted mean oxygen level and trend (1960-2019); its vertical distribution-weighted mean calcite and aragonite saturation states (Ω (Donachy & Watabe, 1986;Dupont et al, 2008Dupont et al, , 2010Wood et al, 2008 (Leys et al, 2004;Whitney et al, 2005) No calcium carbonate (silicious); presumed insensitive to OA (Bindoff et al 2019;Conway et al, 2017); no direct OA studies (Haigh et al, 2015) TA B L E 2 (Continued) (Austin et al, 2007;Leys et al, 2007) Sensitive to but tolerant of low O 2 (Leys & Kahn, 2018); influences population structure (Zeng et al, 2020); rare at O 2 ~<1.4-2.1 ml/L (Leys et al, 2004;Whitney et al, 2005) No calcium carbonate (silicious); presumed insensitive to OA (Bindoff et al 2019;Conway et al, 2017); no direct OA studies (Haigh et al, 2015) All TA B L E 2 (Continued) the three shallowest seamounts, while the undulated glass sponge inhabited all four (S5).…”

“…The keystone brittle star Ophiothrix fragilis is especially sensitive to OA, with 100% mortality of larvae with a modest increase in acidity (pH = 7.9; Dupont, Havenhand, Thorndyke, Peck, & Thorndyke, 2008). In a recent seascape genetics study, water chemistry in the North Atlantic was identified as a driver of genetic variability in cold water coral and sponge populations (Zeng, Rowden, Clark, & Gardner, 2020), indicating changes in Ω (and oxygen) over space and time could influence population connectivity and structure by creating or removing genetic barriers.…”

Does marine geospatial/environmental variation affect genetic variation? A meta-analysis

“…This is one reason why scientists worldwide should pay special attention to the understanding of environmental data and its collection, because this information can give rise to significant predictors for the observed genetic variability. Among other uses, this can provide valuable information for decision making related to marine organisms, i.e., setting of management areas for conservation (Zeng et al, 2020).…”

“…Subsequently, Silva & Gardner (2016) reported for the New Zealand scallop (Pecten novaezelandiae) that variation in population genetic structure was associated with variation in localised freshwater input and suspended particulate matter concentration. Finally, Zeng et al (2020), working with four deep-sea species in the New Zealand region reported a relationship between variation in dissolved oxygen and genetic variation for a sponge (Poecillastra laminaris), and between dynamic topography (Goniocorella dumosa), sea surface temperature (Madrepora oculata) and tidal current (Solenosmilia variabilis) for genetic variation in three cold-water corals. These studies provide valuable new insights into the key environmental drivers of genetic differentiation among populations, setting a precedent for future research worldwide.…”