An Empirical Test of Predictions of Two Competing Models for the Maintenance and Fate of Hybrid Zones: Both Models Are Supported in a Hard-Clam Hybrid Zone

Abstract

Two models developed to discern the mode of selection in hybrid zones differ in some predictions. The tension-zone model predicts that selection acts against hybrids and independently of the environment (endogenous selection) and that selection is invariant throughout the hybrid zone. The ecological selection-gradient, or ecotone, model maintains that fitness of different genotypes varies in response to environmental variation (exogenous selection) and thus, that in a region of the zone, fitness of hybrids is at least equal to that of the parental species. Therefore, to assess the predominant mode of selection operating in a hybrid zone, it is fundamental to evaluate whether selection is acting specifically against hybrid individuals, that is, whether hybridity alone is the basis for deficiencies of hybrids, and to evaluate whether the relative fitness of hybrids versus that of pure species varies across the zone. In a hardclam (genus Mercenaria) hybrid zone located in a polyhaline lagoon in east-central Florida, we used age-specific and location-specific analyses to determine that a hybrid deficit occurrs, that the deficit seems to be due to selection against hybrids, and that selection varies across the zone. Various measures of deviation from Hardy-Weinberg equilibrium, linkage disequilibrium analyses, and shifts in allele frequencies at semidiagnostic loci support the idea that selection is strongest in the northern region of the lagoon, the zone of sympatry and hybridization. Southward, into the range of M. mercenaria (the numerically predominant species), the percentage of hybrids remains relatively high and selection against hybrids decreases. For some genetic linkage groups, selection for M. mercenaria alleles seems to be occurring, but selection seems to be acting principally against alleles characteristic of M. mercenaria and, to a lesser degree, for alleles characteristic of M. campechiensis (the rarer species). These findings and others from previous analyses we have done on this hybrid zone demonstrate that selection in the zone is complex, and that characteristics of both the tension-zone and ecotone models are present. Supporting the tension-zone model, selection against hybrids per se clearly occurs, but specific genotypes seem to be at a selective disadvantage, whereas others have a selective advantage, and selection operates differentially on the two parental species within the zone. Supporting the ecotone model, the strength of overall selection varies throughout the zone, and environmentally mediated selection in which each species and hybrids have an advantage in specific habitats occurs, but some selection against hybrids is invariant throughout the zone. Thus, the structure and genetic architecture of this hybrid zone appear to be products of a complicated interaction between both types of selective forces cited in the two competing models.

Cryptic Vicariance in Gulf of California Fishes Parallels Vicariant Patterns Found in Baja California Mammals and Reptiles

“…Although the aggregate pattern is compelling, there is substantial variance among species in terms of the degree of genetic partitioning and the exact location of genetic breaks. It is likely that contemporary processes have modified each species' imprint of past vicariance (Bert and Arnold 1995;Hare et al 1996), just as both contemporary and historic processes are likely to have affected the genetic differentiation of Gulf of California fishes.…”

“…Although I argued earlier that selection in the absence of vicariance was insufficient to explain the observed patterns, environmentally mediated selection could retard genetic homogenization following secondary contact (Bert and Arnold 1995;Sotka et al 2004). For example, if upper and central Gulf populations have become adapted to local conditions, then there may be considerable exogenous selection against migrant individuals (Barton and Bengsston 1986), and if migrant individuals do not survive to reproduce then gene flow between regions should be low.…”

Isotope sclerochronology of Mercenaria mercenaria, M. Campechiensis, and their natural hybrid form: Does genotype matter?

“…Standard procedures in Bert et al (1993) and later modified by Arnold et al (2004) were followed. We used species-specific standards of hard clam samples previously collected from coastal waters of Connecticut, North Carolina, and the eastern coast of Florida as putative pure species Mercenaria mercenaria and from coastal waters of Texas and northwestern Florida as putative pure species M. campechiensis (Bert and Arnold, 1995). The shells were used for ontogenetic age determination following the methods of Arnold et al (2004).…”

An Integrated Framework for Hybrid Zone Models

“…Each model assumes a particular type of selection on hybrids, but even well-studied zones may be controversial with respect to which models they best fit (Arnold 1997), whereas other studies recognize that their system may be consistent with multiple models (Arntzen and Wallis 1991;Bert and Arnold 1995). One of the models, evolutionary novelty, is a special case that can involve selection both against and for hybrids; the direction is dependent on environment and genotype, rather like a mosaic zone, and this model can occur with any type of hybridization event if novel genotypes arise (Campbell and Waser 2007).…”

“…First, hybrids are generally assumed to be fit or unfit in particular traits regardless of geographic location (despite genotype-by-environment interactions being studied in other contexts: Ingleby et al 2010). Ongoing efforts towards specifying the geographic landscape of fitness (Abbott et al 2013;Bert and Arnold 1995;Martin and Wainwright 2013a;Nosil 2013) are helpful in expanding our understanding of variations in hybrid fitness at different spatial scales, and a few studies have classified hybrid zones by the extent of overlap (Woodruff 1973) or by specifying hybrid fitness by geography (Campbell and Waser 2007). Secondly, clinal (tension zone and bounded hybrid superiority) and mosaic models specify different geographic arrangements of the meeting populations (as in Marshall et al 2002), but the difference between the two classes of model is a matter of environmental grain size (see fig.…”