2015AoB PlantsOpen access

Increased heterosis in selfing populations of a perennial forb

Christopher G. Oakley, Jonathan P. Spoelhof, Douglas W. Schemske

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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.

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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.

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Available 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.

Key concepts: Inbreeding depression, Selfing, Biology, Heterosis, Genetic load, Outcrossing, Population fragmentation, Population

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