Heterosis and Outbreeding Depression in Interpopulation Crosses Spanning a Wide Range of Divergence

Abstract

The intertidal copepod Tigriopus californicus was used as a model organism to look at effects of crossing distance on fitness and to investigate the genetic mechanisms responsible. Crosses were conducted between 12 pairs of populations spanning a broad range of both geographic distance (5 m to 2007 km) and genetic distance (0.2% to 22.3% sequence divergence for a 606-bp segment of the mitochondrial COI gene). For each pair of populations, three fitness components (hatching number, survivorship number, and metamorphosis number) were measured in up to 16 cohorts including parentals, reciprocal F , F , F , and first-generation backcross hybrids. Comparisons of each set of cohorts allowed estimation of within- and between-locus gene interaction. Relative to parentals, F hybrids showed a trend toward increased fitness, with no correspondence with population divergence, and a decrease in variance, which in some cases correlated with population divergence. In sharp contrast, F hybrids had a decrease in fitness and an increase in variance that both corresponded to population divergence. Genetic interpretation of these patterns suggests that both the beneficial effects of dominance and the detrimental effects of breaking up coadaptation are magnified by increasing evolutionary distance between populations. Because there is no recombination in T. californicus females, effects of recombination can be assessed by comparing F hybrid males and females backcrossed to parentals. Both recombinant and nonrecombinant backcross hybrids showed a decline in fitness correlated with population divergence, indicating that segregation among chromosomes contributes to the breakup of coadaptation. Although there was no difference in mean fitness between the two backcross types, recombinational backcrosses showed greater variance for fitness than nonrecombinational backcrosses, suggesting that the breakup of parental gene ombinations within chromosomes has both beneficial and detrimental effects.

Genomic compatibility occurs over a wide range of parental genetic similarity in an outcrossing plant

“…Fenster & Galloway (2000) found heterosis in outbred F 1 plants and hybrid breakdown in the F 3 generation independent of geographical distance. Edmands (1999) also found no relationship between fitness and geographical or genetic distance in the F 1 of a marine copepod, but decreased fitness measures with increasing geographical and genetic distance in the F 2 . These studies show that the pattern of optimal outbreeding may change between F 1 and later generations.…”

“…On the other hand, two sequential generations of outbreeding between populations or species is unrealistic because the F 2 and later generations probably consist of backcrosses with individuals of a parental population. In this case, hybrid breakdown is less likely (Edmands 1999;Schweitzer et al 2002).…”

The Future of Baltic Sea Populations: Local Extinction or Evolutionary Rescue?

“…In this way, hybridization may increase the potential for evolutionary rescue in this species. However, hybridization may also have negative consequences (so called outbreeding depression) during which introduced alleles destroy genetic complexes promoting local adaptation (Edmands 1999).…”

Heterosis and outbreeding depression in crosses between natural populations of Arabidopsis thaliana

“…This approach could also be used to inform conservation genetic strategies, where predicting the success of genetic rescue efforts is of critical importance (Frankham et al, 2011). Line cross techniques have successfully been applied to understanding the genetic architecture of fitness in crosses between natural populations in a variety of taxa, including crustaceans (Edmands, 1999), insects (Armbruster et al, 1997;Demuth and Wade, 2007) and plants (Fenster and Galloway, 2000). Most of these examples uncovered both beneficial dominance effects and negative epistatic effects, at least in some environments.…”

“…Many mildly deleterious recessive or nearly recessive mutations are predicted to become fixed when effective population sizes are modest and gene flow is limited (Whitlock et al, 2000). Heterosis in F 1 crosses between natural populations is ubiquitous (for example, Fenster, 1991;Armbruster et al, 1997;Edmands, 1999;Oakley and Winn, 2012).…”