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Keywords:

  • allozyme;
  • blood groups;
  • genetic relationships;
  • MHC;
  • microsatellite;
  • neutrality;
  • selection

Abstract

  1. Top of page
  2. Abstract
  3. Revisiting neutrality
  4. Revisiting selection
  5. References

Given over 90 combined years in academic and professional activities related to genetics and fishery management (FU 57, JS 36—see Waples et al. 2008), we are pleased to provide an invited perspective generated by the interesting and useful article of McCusker & Bentzen (2010). These authors reaffirm the apparent signature of neutrality of mitochondrial and microsatellite markers through an exhaustive analysis of archived genotypic data for 105 marine and freshwater fishes. They note that their conclusions are consistent with earlier and less comprehensive analyses and that they do not exclude the operation of some selective activity (e.g. genetic ‘draft’), which may be overwhelmed by Ne-related stochastic processes. Here, we provide a complementary focus, recalling relevant issues related to neutrality and selection in applications of molecular variations in fishery management.


Revisiting neutrality

  1. Top of page
  2. Abstract
  3. Revisiting neutrality
  4. Revisiting selection
  5. References

The effective use of allelic blood group markers to clarify human population structures during the 1940s (Cavalli-Sforza & Bodmer 1971) predated relating DNA to protein synthesis (Watson & Crick 1953) and guided fishery scientists towards similar applications (Ridgway 1962). The concept of fishery management through identified population substructures germinated during the 1960s, although because of technological limitations, allelic variants detected by protein electrophoresis (allozymes) displaced blood grouping efforts (Utter et al. 1974). Implicit in these early efforts was an assumption that detected divergence and genetic isolation were directly related; that is, an overall neutral signature of the involved allelic markers. Based on extensive empirical data, a null hypothesis of neutrality rather than selection was adopted as the most reasonable expectation when interpreting large sets of allozyme data (Ihssen et al. 1981). This assumption has been amply validated (e.g. Waples et al. 2004; Utter 2005; Aguilar 2006).

Vigorous, persisting and polarizing challenges to these applications have emerged. Predominating these objections has been a paradigm anticipating temporal instability (and thus unreliability as population markers) of any allelic variants that may be affected by selection. Clinal allozyme variation reported for American eels Anguilla rostrata (Williams et al. 1973) was attributed to strong selection because of a presumed panmictic oceanic parent population. This conclusion was extrapolated to generality by these authors; i.e. ‘…the recognition of separate Mendelian populations on the basis of significantly different allele frequencies in a number of other commercially important species is highly questionable…”.

Extending the observations in American eels, a temporally unstable population structure of European eels Anguilla anguilla also has been revealed by (presumed neutral) microsatellite markers (Dannewitz et al. 2005). Still awaiting full explanation, ‘sweepstakes’ reproductive dynamics (Hedgecock 1994) suggested as a contributing mechanism presents a testable and neutral interpretation of the observed patterns in both species. Nevertheless, the strong selection guideline of Williams et al. (1973) has retained viability, and an underlying fervour that strong selection on molecular genetic variants precludes their effective applications as population markers has been expressed in the literature by such advocates. These beliefs have been concisely expressed by ‘…The selection versus neutralist issue is central to the idea of genetically isolated stocks. Any biological character whose distribution is controlled by selection cannot be used in the identification of isolated stocks…’ (Gauldie 1992). This false dichotomy brings to mind the similarly restrictive ‘God or Darwin’ alternatives presently stifling more constructive scientific and educational searches for reality and truth.

Revisiting selection

  1. Top of page
  2. Abstract
  3. Revisiting neutrality
  4. Revisiting selection
  5. References

The distribution of human blood groups that initially attracted fishery geneticists contains an important clue that was missed during the height of the neutralist–selectionist debate. Since 1943, the Rh blood group system has been implicated in strong selection based on prenatal-induced incompatibilities (Levine 1943). However, prior to the deluge of molecular markers that has accelerated over the past 50 years, this system provided the greatest discrimination for human relationships among five blood group loci (Cavalli-Sforza & Edwards 1963). Clearly evident in Fig. 1 is the consistency of these early suggestions of human relationships with those indicated by contemporary (and putatively neutral) microsatellite markers (Agrawal & Khan 2005).

image

Figure 1.  Clusterings of human population groups based on allelic variation at (left) five blood group loci, from Figure 11.3 in Cavalli-Sforza & Edwards (1963) and (right) five microsatellite loci, from Figure 1b in Agrawal & Khan (2005).

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More recently, data have accumulated for increased rather than reduced discriminatory powers of loci under selection in fish. Particularly fruitful in salmonids has been the major histocompatibility complex (MHC) where, relative to microsatellite loci, greater rather than reduced divergence has been reported in multiple species (reviewed in Evans et al. 2010). In Chinook salmon Oncorhynchus tshawytscha, divergences for two MHC regions relative to those estimated by microsatellite loci were increased for MHC class I but decreased for MHC class II markers, consistent with respective divergent and balancing selective mechanisms (Evans et al. 2010). Indeed, such contrasts were anticipated by Ferguson (1994), and their occurrence in such diverse fishes as stickleback Gasterosteus aculeatus (Hohenlohe et al. 2010), Atlantic cod Gadus morhua (Bradbury et al. 2010) and guppies Poecilia reticulata (Willing et al. 2010) extends the generality of these differences. These congruent patterns in fish and humans strengthen the assumption of Ihssen et al. (1981) of an overall signal of neutrality as a first approximation of reality at the genomic level, as balanced by divergent, convergent and nonselective forces.

As the decodings of multiple genomes become more and more complete and routine, the revelations of McCusker & Bentzen (2010) promise to be further refined rather than rebutted. This process invokes humility rather than arrogance, affirming the paradox that all advancement in scientific understanding inevitably reveals even greater levels of ignorance. As deeper understanding of genomic interactions emerges from within individuals to the entirety of life—past, present and future—inevitably great scientific adventures await investigators throughout and well beyond the 21st century.

References

  1. Top of page
  2. Abstract
  3. Revisiting neutrality
  4. Revisiting selection
  5. References
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