Genetic monitoring of two decades of hybridization between allis shad (Alosa alosa) and twaite shad (Alosa fallax)

Abstract

Habitat alteration has been implicated in driving hybridization between the sympatric migratory shads Alosa alosa and Alosa fallax. Morphological and molecular evidence is consistent with hybridization across the overlapping range of these species, but the temporal extent of hybrid occurrence and genetic consequences for populations have not been explored. Using eight nuclear microsatellite loci and samples collected between 1989 and 2008 in the Solway Firth (UK), we genetically identified hybrids, studied temporal changes in their frequency, and explored changes in allele frequencies of parental populations. These molecular data confirmed the hybrid status of individuals identified using morphology (number of rakers on the outer gill arch), and enabled separation of hybrids from purebred individuals. Mitochondrial cytochrome-b sequencing revealed the presence of two haplogroups, each predominantly occurring in one species. Heterospecific haplotypes were found in 22.3 and 12.8% of A. alosa and A. fallax individuals, respectively, consistent with backcrossing and suggesting that hybrids are fertile. On average, microsatellite-identified hybrids comprised 12.7% of all samples, but when individuals with cytonuclear discordance were also considered introgressed on average 25.4% of individuals were of hybrid ancestry. Overall, allelic richness remained largely unchanged within species, but there were declines in the inbreeding coefficient (F IS ) of both species and episodes of significant temporal allelic frequency change. Hybrids sampled between 2004 and 2008 showed no evidence of lower fecundity relative to purebred individuals. Together, results suggest that hybridization between shad species in northern Europe is prevalent, and has been ongoing over at least two decades. The challenge is now to understand the extent to which observed patterns are linked to immigration from other populations, and the mechanisms that have prevented species collapse despite apparent hybrid fertility and longstanding introgression of neutral markers.

Variable outcomes of hybridization between declining Alosa alosa and Alosa fallax

“…These third-generation hybrids, which cannot be identified using traditional morphological methods, still harbor a significant proportion of genes from the other species (typically an average of 12.5%). This is of great evolutionary significance as it promotes genetic variation within interacting species at a higher rate than the effect of mutation (Anderson, 1953;Hedrick, 2013 (Coscia et al, 2010) and of the Solway Firth (Jolly et al, 2011) and in the present study across the French Atlantic coast or toward A. fallax in Portugal . These results highlight the potential for substantial variability in the genetic consequences of hybridization in Eurasian shads.…”

Comparative phylogeography and demographic history of European shads (Alosa alosa and A. fallax) inferred from mitochondrial DNA

“…In particular, given the limited number of samples analyzed per species in phylogenetic studies [25,26], it is not clear if the monophyletic status of European shad species will be maintained with increased geographic sampling coverage. Moreover, despite the identification of significant genetic differentiation between populations, mainly among A. fallax populations, some studies have a very regional focus [31,32], while others are based on genetic markers with limited variability for drawing broad geographic-scale conclusions (e.g. [28,30]), highlighting the need for a comprehensive phylogeographic study.…”

Delimitation of Alosa species (Teleostei: Clupeiformes) from the Sea of Azov: integrating morphological and molecular approaches

“…The relatively large divergence of mtDNA sequences compared with the genome‐wide set of SNPs from the Sea of Azov specimens could have resulted from an introgressive hybridization event such as has been reported for the closely related Mediterranean species A. fallax and A. alosa (Alexandrino et al, ; Coscia et al, ; Faria et al, ; Jolly et al, ). It is conceivable that introgressive contact may have occurred between different species due to their limited spawning area in the Sea of Azov together with the inaccessibility and disturbance of their preferred spawning grounds by dams that block upstream migrations of the anadromous Alosa spp., forcing them to share spawning sites with semi‐anadromous congeners.…”

“…Despite the economic significance of the genus Alosa , species delimitation within the group is challenging due to high interspecific morphological similarity, complex population structure and intraspecific phenotypic plasticity (Alexandrino et al, ; McDowall, , ) and interspecific hybridization (Alexandrino et al, ; Faria et al, ; Jolly et al, ; McBride et al, ). Within the Mediterranean and north‐east Atlantic group, status of the species Alosa fallax (Lacepéde 1803) and Alosa alosa (L. 1758) has historically been a subject of contention due to their close genetic relationships and extensive hybridization (Alexandrino et al, ; Boisneau et al, ; Coscia et al, ; Faria et al, ).…”

“…Delimitation of some North American species has also been problematic, especially for the morphologically similar species Alosa pseudoharengus (Wilson 1811) and Alosa aestivalis (Mitchill, 1814), Alosa sapidissima (Wilson 1811) and Alosa alabamae Jordan & Evermann, 1896, as well as for delimiting ecomorphs within species (Chapman et al, 1994;Czesny et al, 2012;Nolan et al, 2003). Current understanding of the evolutionary relationships and taxonomy of North American, Mediterranean and northern European species of Alosa has been advanced with extensive molecular studies Bowen et al, 2008;Czesny et al, 2012;Faria et al, 2006Faria et al, , 2011Faria et al, 2004Faria et al, , 2012Hasselman et al, 2013;Jolly et al, 2011Jolly et al, , 2012; however, the Ponto-Caspian assemblage of Alosa species remains understudied. Relatively few molecular studies have investigated genetic interrelationships of Alosa spp.…”