Abstract
Quantifying the importance of random genetic drift in natural populations is central to understanding the potential limits to natural selection. One approach is to estimate the magnitude of heterosis, the increased fitness of progeny derived from crosses between populations relative to crosses within populations caused by the heterozygous masking of deleterious recessive or nearly recessive alleles that have been fixed by drift within populations. Self-fertilization is expected to reduce the effective population size by half relative to outcrossing, and population bottlenecks may be common during the transition to selfing. Therefore, chance fixation of deleterious alleles due to drift in selfing populations should increase heterosis between populations. Increased homozygosity due to fixation or loss of alleles should also decrease inbreeding depression within populations. Most populations of the perennial herb Arabidopsis lyrata ssp. lyrata are self-incompatible (SI), but several have evolved self-compatibility and are highly selfing. We quantified heterosis and inbreeding depression in two predominantly self-compatible (SC) and seven SI populations in a field common garden experiment within the species' native range and examined the correlation between these metrics to gauge the similarity in their genetic basis. We measured proportion germination in the lab, and survival and fecundity (flower and seed production) for 2 years in the field, and calculated estimates of cumulative fitness. We found 7.2-fold greater heterosis in SC compared with SI populations, despite substantial heterosis in SI populations (56 %). Inbreeding depression was >61 %, and not significantly different between SC and SI populations. There was no correlation between population estimates of heterosis and inbreeding depression, suggesting that they have somewhat different genetic bases. Combined with other sources of information, our results suggest a history of bottlenecks in all of these populations. The bottlenecks in SC populations may have been severe, but their strong inbreeding depression remains enigmatic.
Highlights
Understanding the causes and consequences of differentiation among natural populations is a central goal in evolutionary biology
We address the following questions: (i) What are the magnitudes of heterosis in SC and SI populations? (ii) How does the magnitude of heterosis vary across the life cycle, and what might that tell us about its genetic basis? (iii) What is the magnitude of cumulative inbreeding depression in SC vs. SI populations, and what is the relationship between population mean inbreeding depression and heterosis?
Because all of these populations occupy regions that were glaciated during the Pleistocene and show reduced levels of neutral genetic variation compared with populations from the centre of the range (Griffin and Willi 2014), we suggest that a history of population bottlenecks is a plausible explanation for at least part of the observed heterosis
Summary
Understanding the causes and consequences of differentiation among natural populations is a central goal in evolutionary biology. While much attention has been given to the effects of natural selection, random genetic drift can be important in shaping patterns of genetic variation. An increase in progeny fitness following betweenpopulation relative to within-population crosses is thought to be caused by the heterozygous masking (in the F1) of mildly deleterious, partly recessive alleles historically fixed by drift in the parental populations. Increased performance or yield in crosses due to heterosis has long been of interest in plant and animal breeding (Hochholdinger and Hoecker 2007; Lippman and Zamir 2007; Chen 2010), but its value for studying the causes and consequences of reductions in effective population sizes in natural populations has been underappreciated
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