Objective 2: Meta-review of fish taxa
Sticklebacks
Research on sticklebacks has focused primarily on one species, the threespine stickleback, Gasterosteus aculeatus , with fewer studies on ninespine stickleback, Pungitius pungitius (e.g., Table 2). Within species, the divergence of populations is suggestive of population structuring. The threespine stickleback has been a model organism for studying behavior, host-parasite relationships, morphology, evolutionary ecology, and speciation (e.g., Bell and Foster 1994; McKinnon and Rundle 2002; Baker et al. 2008; Hendry et al. 2009, 2013; Wootton 2009; Schluter 2010). The overall trend with studies on the threespine stickleback has been the identification of numerous species, followed by lumping into one species, followed by a return to splitting the phenotypes back out into individual species in some geographical areas.
In the early 1900s, taxonomists struggled with the wide phenotypic diversity of threespine stickleback and several phenotypes were initially believed to be separate species (Wootton 2009). This diversity is captured in the following quote: “Race ranking may be accorded forms, like local types of Gasterosteus aculeatus , which are so confusingly numerous or so complex in characters, and so complicated in genetic and geographical relationship, as to transcend any ordinary scheme of zoological nomenclature” (Hubbs 1943). It has since been argued that the threespine stickleback is a “raceme” (persistent lineage [marine phenotype] out of which multiple lineages [anadromous and freshwater phenotypes] diverge and quickly end in extinction) or “species complex”, composed of thousands of diverse populations that have evolved numerous times in particular locations (Bell and Foster 1994; Schluter and Conte 2009; Wootton 2009; Hendry et al. 2013). Others refer to the diversity within threespine stickleback by calling the species a “superspecies” (Baker et al. 2008).
Stickleback speciation is complex and involves multiple traits. This speciation occurs rapidly in diverse geographical areas. Natural selection, sexual selection, standing genetic variation, mutation, and genetic recombination have led to rapid reproductive isolation and speciation that has occurred since the last glaciers ca. 9,000 – 13,000 years ago (McKinnon and Rundle 2002; Schluter and Conte 2009; Wootton 2009; Schluter 2010; Hendry et al. 2013). In the mid- to late-1900s, research on sticklebacks examined the variation and adaptive significance of phenotypic traits including body shape and size, body armor (bony plates), spines and skeletal structure, spawning coloration, life history characteristics, and behavior. In the latter part of this period, research focused on the adaptive radiation and reproductive isolation of sticklebacks in lakes. In the 2000s, genomic studies on sticklebacks revealed insights into associations between phenotype, genotype, and selective factors (Wootton 2009).
Phenotypic and genotypic differences in threespine stickleback have been found among marine, anadromous, freshwater resident populations (lakes and streams), and between phenotypes within these habitats (e.g., limnetic vs. benthic phenotypes/species; Table 2). This diversity has been identified as “species pairs” (Taylor 1999; Hendry et al. 2009; Wootton 2009), “ecomorph pairs” (Wootton 2009), and “ecotypes” (Table 2; Taylor 1999; Hendry et al. 2013), although life history diversity has been examined and so “life history” has also been used (Table 2; Baker et al. 2008). Some of these phenotypes of threespine stickleback show sufficient reproductive isolation and phenotypic and genotypic differences to warrant calling them separate species, although they still bear the same scientific name (Wootton 2009; Schluter 2010). For example, “limnetic” and “benthic” phenotypes/species have been shown to be adaptive in the littoral zone (benthic species/phenotype) and limnetic zone (limnetic species/phenotype) within some lakes (Schluter 2010) and phenotypes associated with different lake substrates (lava vs. mud; Kristjánsson et al. 2002) in ways that reduce competition for resources (Schluter 2010). In addition, some phenotypic and genotypic divergence in lakes has been attributed to predators and prey (Millet et al. 2013; Miller et al. 2019), and parasitism may also influence divergence leading to speciation between limnetic and benthic threespine sticklebacks (Schluter 2010).
The appropriate terminology for describing threespine stickleback diversity may depend on the population(s) in question. This is because speciation within sticklebacks occurs along a continuum, from “continuous variation within panmictic populations” on one end to “complete and irreversible reproductive isolation” on the other, with factors affecting the divergence of populations along this continuum (Hendry et al. 2009). Hendry et al. (2009) reported that most stickleback populations are on the front end of this spectrum, “…even though some of these [populations] show evidence of disruptive selection and positive assortative mating”.