Can spatial sorting associated with spawning migration explain evolution of body size and vertebral number inAnguillaeels?

Abstract

Spatial sorting is a process that can contribute to microevolutionary change by assembling phenotypes through space, owing to nonrandom dispersal. Here we first build upon and develop the “neutral” version of the spatial sorting hypothesis by arguing that in systems that are not characterized by repeated range expansions, the evolutionary effects of variation in dispersal capacity and assortative mating might not be independent of but interact with natural selection. In addition to generating assortative mating, variation in dispersal capacity together with spatial and temporal variation in quality of spawning area is likely to influence both reproductive success and survival of spawning migrating individuals, and this will contribute to the evolution of dispersal‐enhancing traits. Next, we use a comparative approach to examine whether differences in spawning migration distance among 18 species of freshwater Anguilla eels have evolved in tandem with two dispersal‐favoring traits. In our analyses, we use information on spawning migration distance, body length, and vertebral number that was obtained from the literature, and a published whole mitochondrial DNA‐based phylogeny. Results from comparative analysis of independent contrasts showed that macroevolutionary shifts in body length throughout the phylogeny have been associated with concomitant shifts in spawning migration. Shifts in migration distance were not associated with shifts in number of vertebrae. These findings are consistent with the hypothesis that spatial sorting has contributed to the evolution of more elongated bodies in species with longer spawning migration distances, or resulted in evolution of longer migration distances in species with larger body size. This novel demonstration is important in that it expands the list of ecological settings and hierarchical levels of biological organization for which the spatial sorting hypothesis seems to have predictive power.

Ecological and Evolutionary Consequences of Environmental Change and Management Actions for Migrating Fish

“…Species showing pronounced intraspecific variation include some salmonids (S. trutta), the three-spine stickleback (Gasterosteus aculeatus), and the northern pike (Esox lucius) in which different populations of the same species can be classified as belonging to at least two of the oceanodromous, potamodromous, and the anadromous lifestyles (Jonsson and Jonsson, 1993;Fleming, 1996;Lucas and Baras, 2001;Dodson et al, 2013;Forsman et al, 2015;Leitwein et al, 2016). There is also extensive variation in timing and distance of migration among species and populations (McDowall, 1997;Hendry and Day, 2005;Kuparinen and Merilä, 2009;Griffiths, 2010;Seamons and Quinn, 2010;Kovach et al, 2015;Forsman and Berggren, 2017;Bloom et al, 2018).…”

“…Patterns and strategies of migration vary extensively among species with regards to function (e.g., spawning, feeding, and refuge from predators and other environmental stressors), migration mode (diadromous, potamodromous and oceanodromous), mode of parity (semelparous-iteroparous), timing of migratory events (phenology), and migratory distance (McDowall, 1997;Griffiths, 2010;Seamons and Quinn, 2010;Mehner, 2012;Forsman and Berggren, 2017;Nilsson et al, 2019). As for diadromy, inter-specific comparisons have uncovered that anadromous species predominate in temperate latitudes where productivity in freshwater is generally lower than in marine environments whereas catadromy dominates in tropical latitudes where the highest productivity is found in freshwater habitats (Gross et al, 1988;McDowall, 1997).…”

“…For pike, maximum migration distance in freshwater is probably < 50 km (Larsson et al, 2015), whereas the goliath catfish that spawns in the western Amazon travels 11,500 km, the longest fish freshwater migration in the world (Barthem et al, 2017). In the catadromous Anguilla eels, migration distances from freshwater to the marine spawning areas range from 750 to > 8,000 km (see Table S1 in Forsman and Berggren, 2017). Results from a comparative analysis indicate that the evolutionary increments of migration distances in Anguilla have been accompanied by shifts in dispersal enhancing phenotypic traits, such as larger body size (Forsman and Berggren, 2017).…”

Inter‐individual variation in colour patterns in noctuid moths characterizes long‐distance dispersers and agricultural pests

“…One way to identify proxies for dispersal capacity is to use indirect estimates based on traits that are thought, or proven, to be associated with differences in dispersal capacity. Earlier studies have indicated a number of species traits and ecological characteristics as related to dispersal capacity in a wide range of organisms, such as hind-foot length in voles (Forsman, Merilä, & Ebenhard, 2011;Shine, Brown, & Phillips, 2011), wing length in birds and insects (Berggren, Tinnert, & Forsman, 2012;Rundle, Bilton, Abbott, & Foggo, 2007;Sekar, 2012;Stevens et al, 2010), and body size in eels (Forsman & Berggren, 2017).…”

The role of habitat choice in micro‐evolutionary dynamics: An experimental study on the Mediterranean killifish Aphanius fasciatus (Cyprinodontidae)

“…Despite its potential role in micro‐ and macro‐evolutionary processes and the increasing recognition that genotypes can differ in dispersal ability or in habitat preference (Rice, ; Canestrelli et al., ; Forsman & Berggren, ), habitat choice is still an overlooked issue in evolutionary ecology (Edelaar et al., ). Indeed, habitat choice has been rarely evoked to explain the genetic patterns of natural populations (e.g., Byers, , ; Borowsky, ; Szarowska, Falniowski, Mazan, & Fialkowski, ), likely because field studies make it difficult to disentangle the patterns of genetic divergence originated by habitat choice from those due to the action of other diverging forces, such as drift or selection.…”