Rapid divergence of mussel populations despite incomplete barriers to dispersal

Abstract

Striking genetic structure among marine populations at small spatial scales is becoming evident with extensive molecular studies. Such observations suggest isolation at small scales may play an important role in forming patterns of genetic diversity within species. Isolation-by-distance, isolation-by-environment and historical priority effects are umbrella terms for a suite of processes that underlie genetic structure, but their relative importance at different spatial and temporal scales remains elusive. Here, we use marine lakes in Indonesia to assess genetic structure and assess the relative roles of the processes in shaping genetic differentiation in populations of a bivalve mussel (Brachidontes sp.). Marine lakes are landlocked waterbodies of similar age (6,000-10,000 years), but with heterogeneous environments and varying degrees of connection to the sea. Using a population genomic approach (double-digest restriction-site-associated DNA sequencing), we show strong genetic structuring across populations (range F : 0.07-0.24) and find limited gene flow through admixture plots. At large spatial scales (>1,400 km), a clear isolation-by-distance pattern was detected. At smaller spatial scales (<200 km), this pattern is maintained, but accompanied by an association of genetic divergence with degree of connection. We hypothesize that (incomplete) dispersal barriers can cause initial isolation, allowing priority effects to give the numerical advantage necessary to initiate strong genetic structure. Priority effects may be strengthened by local adaptation, which the data may corroborate by showing a high correlation between mussel genotypes and temperature. Our study indicates an often-neglected role of (evolution-mediated) priority effects in shaping population divergence.

Landscape genetic structure of Scirpus mariqueter reveals a putatively adaptive differentiation under strong gene flow in estuaries

“…Genetic structure in S. mariqueter also could reflect "isolation by population history" which has been evidenced by recently studies (Maas et al, 2018). This mode of isolation emphasize the importance of colonizers in shaping subsequent population genetic structure, also termed "historical priority effects" (Maas et al, 2018;De Meester, Vanoverbeke, Kilsdonk, & Urban, 2016) or "historical contingency" (Fukami, Mordecai, & Ostling, 2016;Orsini, Vanoverbeke, Swillen, Mergeay, & Meester, 2013) It is meaning that the early colonizers tend to be more locally adapted in comparison with late arrivers, due to density-dependent and evolution-mediated dominance of early genotypes. For example, there is not a complete barrier in the open sea, as the water/ocean currents can carry propagules among estuarine populations.…”

“…Such characteristics indicate that individuals who founded the population could originate from multiple source populations rather than from a single source population. However, the successful colonizers are almost the first colonizers due to density‐dependent ecological priority effects which may further mediated by evolution via adaptation to local conditions (Maas et al, ). This observation has been evidenced, and the high plasticity would benefit colonization of new locations.…”

“…For example, on a large geographic scale, the genetic pattern may be the result of historical events or past colonization history (Tahvanainen et al, 2012;Arnaud-Haond et al 2014;Sahyoun, Guidetti, Franco, & Planes, 2016;Maas et al, 2018), but also it may be due to complicated life history (Dennenmoser, Rogers, & Vamosi, 2014;Kesäniemi et al, 2014;Miller et al, 2018) and dispersal behavior (Becquet et al, 2013;Ngeve et al, 2017) as well as physiological or ecological limit to dispersal. In this case, because several different factors acting both spatially and temporally can lead to chaotic patterns in genetic structure, and they are frequently confounded (Maas et al, 2018); it is difficult to clear identify which factors are most important.…”

“…However, there has been complex genetic structure described as "chaotic" in marine environments when it cannot be explained or barriers to dispersal cannot be identified (Toonen and Grosberg 2011;Kesäniemi et al, 2014;Cornwell, Fisher, Morgan, & Neigel, 2016;Norderhaug et al, 2016;Miller, Baird, Oosterom, Mondon, & King, 2018), suggesting that there may be other isolation mode or cryptic limit to dispersal. For example, on a large geographic scale, the genetic pattern may be the result of historical events or past colonization history (Tahvanainen et al, 2012;Arnaud-Haond et al 2014;Sahyoun, Guidetti, Franco, & Planes, 2016;Maas et al, 2018), but also it may be due to complicated life history (Dennenmoser, Rogers, & Vamosi, 2014;Kesäniemi et al, 2014;Miller et al, 2018) and dispersal behavior (Becquet et al, 2013;Ngeve et al, 2017) as well as physiological or ecological limit to dispersal. In this case, because several different factors acting both spatially and temporally can lead to chaotic patterns in genetic structure, and they are frequently confounded (Maas et al, 2018); it is difficult to clear identify which factors are most important.…”

Towards an urban marine ecology: characterizing the drivers, patterns and processes of marine ecosystems in coastal cities

“…Artificial structures has been shown to o act as 'stepping stones' for dispersal, particularly of non-indigenous taxa (Bulleri and Airoldi 2005, Glasby et al 2007, Vaselli et al 2008, Sheehy and Vik 2010, Airoldi et al 2015, Foster et al 2016) and alter genetic population structure of marine fauna (Fauvelot et al 2012). Marine species vary in dispersal potential, and many taxa encounter barriers to dispersal at relatively small spatial scales (Darling et al 2009, Costantini et al 2013, Maas et al 2018, Sefbom et al 2018. Dispersal limitation can therefore also interact with local stressors and abiotic conditions to result in compositionally very different assemblages across patches of hard substrata (Bulleri andChapman 2004, Munari 2013).…”