Patterns of invasion and colonization of the sea lamprey (Petromyzon marinus) in North America as revealed by microsatellite genotypes

Abstract

Invasions by exotic organisms have had devastating affects on aquatic ecosystems, both ecologically and economically. One striking example of a successful invader that has dramatically affected fish community structure in freshwater lakes of North America is the sea lamprey (Petromyzon marinus). We used eight microsatellite loci and multiple analytical techniques to examine competing hypotheses concerning the origins and colonization history of sea lamprey (n = 741). Analyses were based on replicated invasive populations from Lakes Erie, Huron, Michigan, and Superior, populations of unknown origins from Lakes Ontario, Champlain, and Cayuga, and populations of anadromous putative progenitor populations in North America and Europe. Populations in recently colonized lakes were each established by few colonists through a series of genetic bottlenecks which resulted in lower allelic diversity in more recently established populations. The spatial genetic structure of invasive populations differed from that of native populations on the Atlantic coast, reflecting founder events and connectivity of invaded habitats. Anadromous populations were found to be panmictic (theta(P) = 0.002; 95% CI = -0.003-0.006; P > 0.05). In contrast, there was significant genetic differentiation between populations in the lower and upper Great Lakes (theta(P) = 0.007; P < 0.05; 95% CI = 0.003-0.009). Populations in Lakes Ontario, Champlain, and Cayuga are native. Alternative models that describe different routes and timing of colonization of freshwater habitats were examined using coalescent-based analyses, and demonstrated that populations likely originated from natural migrations via the St Lawrence River.

Sea lampreyPetromyzon marinus: an exception to the rule of homing in anadromous fishes

“…This corresponds with our findings of no significant differences ( pO0.05) in haplotypic frequencies among collections in other discrete regions, including native landlocked populations in Lake Ontario (three rivers; Waldman et al 2004), in Lake Champlain (four rivers; Waldman et al 2006) and between two rivers in Portugal ( pZ0.8643; Rodríguez-Muñ oz et al 2004). Moreover, it is congruent with findings from nuclear DNA microsatellite analyses for Atlantic coast anadromous sea lamprey populations and among populations in Lakes Ontario and Champlain (Bryan et al 2005). We hypothesize that this panmixia is one outcome of an alternative life-history strategy from that employed by other anadromous fishes, and that this strategy is directly allied with its parasitism.…”

Mitochondrial DNA fails to reveal genetic structure in sea-lampreys along European shores

“…These findings led Rodriguez-Muñ oz et al (2004) to raise the possibility that the sea-lamprey underwent a severe bottleneck in Southwest Europe. Bryan et al (2005), using microsatellites, also found that in a Portuguese River (Mondego), the genetic diversity was very low when compared with that found in North-western Atlantic rivers, supporting the finding of Rodriguez-Muñoz et al (2004). They suggested that a serious reduction of effective population size may have occurred in Europe as a result of the fisheries that exploit sea-lamprey in several countries.…”

“…This lack of differentiation is not caused by insufficient variability in the markers used, as demonstrated by the differentiation among populations of lakes where the sea lamprey is possibly native (Bryan et al, 2005;Waldman et al, 2006). More likely, the lack of structure in Atlantic rivers results from the lack of homing in this species (Bergstedt and Seelye, 1995).…”

“…Both microsatellites (Bryan et al, 2005) and mtDNA control region (Waldman et al, 2006) revealed a notorious lack of differentiation among the North American rivers draining into the Atlantic. This lack of differentiation is not caused by insufficient variability in the markers used, as demonstrated by the differentiation among populations of lakes where the sea lamprey is possibly native (Bryan et al, 2005;Waldman et al, 2006).…”

“…While in North America it became a serious problem for many aquatic ecosystems after it invaded the great lakes (Bryan et al, 2005), in Western Europe its conservation is raising increasing concerns (Maitland, 2003). Being an adromous, the sealamprey migrates into rivers and must reach gravel streams where spawning takes place.…”