Ecological genomics of divergence, admixture, and fitness in the smallmouth bass (Micropterus dolomieu)

The Smallmouth Bass (Micropterus dolomieu) is one of the most highly targeted sport fishes in the world. Anglers vie for the opportunity to catch Smallmouth Bass recreationally and competitively, spending billions of dollars every year on travel, equipment, and conservation permits. Along with their extreme popularity, they are of central importance in their native ecosystems throughout central and eastern North America. They are voracious apex predators, controlling top-down food web dynamics among fishes and invertebrates in both streams and natural lakes, and they act as obligate hosts in the life cycles of several freshwater mussels. A great deal is known about the general ecology of Smallmouth Bass and their role in aquatic communities across their extensive native distribution. Much less is known about levels and distribution of diversity within the species. In 1940, Carl Hubbs and Reeve Bailey published descriptions of two distinct subspecies: the Northern Smallmouth Bass (M. d. dolomieu), inhabiting the central and eastern portion of the range, and the Neosho Smallmouth Bass (M. d. velox), which is range-restricted to the Arkansas River Basin in the Central Interior Highlands. While the subspecies classification was largely accepted among taxonomists, it was predicated on only a few subtle morphological traits, including differences in coloration, body size, and the presence of glossohyal teeth. Researchers began to investigate genetic divergence among Smallmouth Bass populations at the end of the twentieth century. Some genetic structure has been detected, but the overall diversity and the evolutionary forces generating contemporary patterns have been considered extremely complex and therefore unresolved, especially where the Neosho and Northern subspecies ranges meet in the Central Interior Highlands. To address the need for a robust understanding of the divergence and evolution history of Smallmouth Bass in the Central Interior Highlands, I addressed three broad areas concerning the phylogeography and conservation of the species using a combination of morphological, genetic, and genomic data: 1) patterns of genetic and morphological differentiation between the Neosho and Northern Smallmouth Bass subspecies, 2) lineage diversification and the extent and origins of admixture within the subspecies, and 3) effects of admixture on individual growth and fitness in two streams within the Neosho Smallmouth Bass native range. Using neutral microsatellite markers and a combination of three independent Bayesian analysis methods, I detected complex and hierarchical population structure of Smallmouth Bass in the Central Interior Highlands. The broadest level of structure indicated two distinct genetic clusters corresponding to the Neosho and Northern subspecies, but with substantial and heterogenous patterns of admixture within some streams in the Neosho native range. At finer levels of structure, clusters corresponded to river drainages and to potentially distinct populations within drainages. The Northern and Neosho subspecies were morphologically distinct overall based on principal component analysis of five morphometric traits, but they significantly differed only in head length. Based on genome-wide variation at over 50,000 single nucleotide polymorphisms, the Neosho and Northern subspecies represented two diverged, monophyletic clades, each comprising two additional monophyletic lineages. Populations in Big Piney Creek and the Illinois Bayou within the Neosho range also showed signatures of local adaptation based on outlier FST analysis. Admixture in the Illinois River system within the Neosho range originated from a hatchery strain of Northern Smallmouth Bass found in Skiatook Lake, Oklahoma, while admixture in the Elk River, upper Arkansas River tributaries, and the Illinois Bayou and Big Piney Creek system originated from the White River in the Northern range. Demographic analysis revealed that admixture in these streams has occurred on different time scales, in some cases likely due to historic migration, and in other cases likely due to secondary contact, possibly as a result of anthropogenic introductions. In Big Sugar Creek and the Elk River, two Neosho Smallmouth Bass native streams known to be admixed with White River Northern Smallmouth Bass, individual growth did not differ between genetically pure Neosho, pure Northern, or admixed fish. However, in the Elk River alone, average length-at-infinity (maximum length) was lower for admixed fish than for either pure Neosho or pure Northern fish. We also found a significant negative relationship between multi-locus heterozygosity (based on fourteen microsatellite loci) and body condition, suggesting that increased intermixing may be causing outbreeding depression in these streams. The Neosho and Northern Smallmouth Bass constitute highly differentiated, locally adapted, and independently evolving lineages in the Central Interior Highlands. Despite divergence, there are also complex and extensive patterns of admixture in the Neosho range which may be contributing to lower fitness in two Neosho Smallmouth Bass streams. It will be crucial to consider these patterns and their potential outcomes in the development of management protocols for the preservation of endemic diversity within this economically and ecologically vital sportfish.