Academic journal article Genetics

The Genetic Basis of Developmental Abnormalities in Interpopulation Hybrids of the Moss Ceratodon Purpureus

Academic journal article Genetics

The Genetic Basis of Developmental Abnormalities in Interpopulation Hybrids of the Moss Ceratodon Purpureus

Article excerpt

ABSTRACT

Divergent populations are intrinsically reproductively isolated when hybrids between them either fail to develop properly or do not produce viable offpring. Intrinsic isolation may result from Dobzhansky-Muller (DM) incompatibilities, in which deleterious interactions among genes or gene products lead to developmental problems or underdominant chromosome structure differences between the parents. These mechanisms can be tested by studying marker segregation patterns in a hybrid mapping population. Here we examine the genetic basis of abnormal development in hybrids between two geographically distant populations of the moss Ceratodon purpureus. Approximately half of the hybrid progeny exhibited a severely reduced growth rate in early gametophyte development. We identified four unlinked quantitative trait loci (QTL) that interacted asymmetrically to cause the abnormal development phenotype. This pattern is consistent with DM interactions. We also found an excess of recombination between three marker pairs in the abnormally developing progeny, relative to that estimated in the normal progeny. This suggests that structural differences in these regions contribute to hybrid breakdown. Two QTL coincided with inferred structural differences, consistent with recent theory suggesting that rearrangements may harbor population divergence alleles. These observations suggest that multiple complex genetic factors contribute to divergence among populations of C. purpureus.

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DIVERGENT populations become intrinsically reproductively isolated when hybrids between them either fail to develop properly or do not produce viable offpring. Intrinsic barriers may result from either deleterious interactions among heterospecific genes or gene products or chromosome structure differences that are deleterious in heterozygotes. The genic model, independently proposedbyBateson(1909),Dobzhansky (1937), and Muller (1942) and typically referred to as the Dobzhansky-Muller (DM) model, proposes that complementary alleles at interacting loci have normal fitness in their native genetic background, but low fitness in a heterospecific background. The DM model makes several clear predictions regarding the nature of these deleterious interlocus interactions (reviewed in Coyne and Orr 2004). The simplest DM incompatibility involves interactions between alleles at two loci. Consider an ancestral population of haploids with a two-locus genotype AB. In one daughter population, a derived mutation is fixed at one interacting partner (aB), while in a second daughter population a mutation is fixed at the complementary locus (Ab). The DMmodel proposes that the ab genotype,which has not been tested by natural selection, has a lower fitness. In this example, the ancestral A and B alleles each may be introgressed between the two daughter populations, but the derived a and b alleles cannot. While more complex interlocus interactions may occur, this asymmetry is the hallmark of DM interactions (Orr 1995; Turelli and Moyle 2007). Importantly, the DM model does not imply that a low-fitness valley must be crossed in the process of population divergence.

Alternatively, hybrid F^sub 1^'s between individuals with different karyotypes may have reduced fertility because recombination in rearranged chromosomal segments leads to the production of aneuploid gametes (King 1993). Thus, gametes with parental karyotypes are functional, but recombinant meiotic products often lack chromosome arms or whole chromosomes and generally do not contribute to the next generation. Closely related species frequently differ in karyotype, suggesting that rearrangements may be an important cause of intrinsic isolation (Stebbins 1971; White 1978; King 1993). However, whether such rearrangements contribute to the speciation process is a matter of debate (Sites and Moritz 1987; Coyne and Orr 2004). For a particular rearrangement to fix in a population, it initially must pass through a heterozygous phase where it confers reduced fertility. …

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