Evolution of Phenotypic Diversity in Gasterosteus aculeatus Superspecies on the Pacific Coast of North America

Abstract

Bell, M. A. (Department of Biology, University of California, Los Angeles, Califomnia 90024) 1976. Evolution of phenotypic diversity in Gasterosteus aculeatus superspecies on the Pacific coast of North America. Syst. Zool. 25:211-227.-A conceptual model for the evolution of phenotypic diversity of the threespine stickleback on the Pacific coast of North America is presented. This model takes into account biological characteristics of the threespine sticklebackand climatic changes during Pleistocene times. Biological features considered include: (1) life history patterns in freshwater and anadromous populations; (2) distribution of freshwater and anadromous populations; (3) morphological variation in freshwater populations; (4) genetics of morphological features; (5) the characteristics of highly divergent populations and their distribution in time and space; (6) character displacement. Previous models for the evolution of phenotypic diversity and the interactions of selection and gene flow are considered. Hypotheses concerning protein evolution in Pacific coast sticklebacks are generated from the model. These hypotheses depend on recent evidence that protein evolution does not have a cause and effect relationship with phenotypic divergence and speciation. A causal relationship between the unusual mode of evolution in western North American Gasterosteus and their low haploid DNA content is tentatively suggested. If the model is correct, freshwater subspecies proposed by Miller and Hubbs (1969) for the nominal species Gasterosteus aculeatus are polyphyletic. [Teleostei; Gasterosteidae; speciation.] Gasterosteus aculeatus, the threespine stickleback, appears to be a superspecies composed of semispecies, some of which are polytypic and polymorphic but all of which form a cohesive taxonomic unit. This remarkable diversity led first to an explosive proliferation of nominal species followed by a process of synonymy. Taxonomic questions aside, the evolutionary mechanisms responsible for this phenotypic diversity, restricted within bounds that have not been breached to produce progressive adaptive radiation leading to distinctive, divergent lineages must be complex. It is generally believed that the biological species concept articulated by Mayr (1969) adequately describes the attributes of taxa regarded as species. This concept of species, however, fails to explain the situation characterized by the threespine stickleback. But is the threespine stickleback a rare exception to a generally valid rule? It could be that the threespine stickleback more clearly displays the genetic diversity, which, unperceived in other organisms, has led us to an oversimplified view of the evolutionary unit represented by species. According to the biological species concept, the bond holding together species is gene flow. Among other attributes ascribed to the biological species, Mayr (1969) considered the biological species to be .. . a genetic unit consisting of a large, intercommunicating gene pool,... We find that in Gasterosteus aculeatus, in the absence of gene flow for periods sufficient to allow morphological divergence, morphological divergence seems almost inevitable but usually is held within well defined limits. The vast majority of populations are composed of one or more of Hagen and Gilbertson's (1972) morphs (i.e., low, partial and completely plated), and this is an adequate characterization of them. The criteria for biological species may or may not be attained by divergent populations included within these limits. Populations exceeding these limits may attain the status of biological species, but even among such populations, their phenotypic characteris-