Intraparental Gamete Competition Provides a Selective Advantage for the Development of Hybrid Sterility via Meiotic Drive

Abstract

Hybrid sterility can have evolutionary significance and varies substantially by taxon, but few models attempt to predict or explain this variability. Hybrid sterility is commonly observed and develops early in isolation, at odds with straightforward models that predict it would develop slowly and rarely be seen. Meiotic drive might explain the rapid development of hybrid sterility, but drive is rarely observed, modifiers are expected to repress it, and no precise testable predictions are available. Here I develop population genetic models for the establishment of meiotic drive based on how it spreads by benefiting carrier gametes competing with noncarrier gametes from the same parent, or intraparental gamete competition. The resulting models predict that meiotic drive can often produce substantial hybrid sterility over time even in the presence of repressors, yet observable drive will be rare. They also make quantitative predictions of the degree of sterility based on observable parameters of reproductive ecology, including frequency of multiple mating, effective dispersal of offspring, and population size. Finally, they suggest explanations for the association of heterochromatin changes with speciation. Experimental evidence is discussed showing that drive alleles at least sometimes contribute to hybrid sterility.

TOWARD THE EVOLUTIONARY GENOMICS OF GAMETOPHYTIC DIVERGENCE: PATTERNS OF TRANSMISSION RATIO DISTORTION IN MONKEYFLOWER (MIMULUS) HYBRIDS REVEAL A COMPLEX GENETIC BASIS FOR CONSPECIFIC POLLEN PRECEDENCE

“…In addition to its obvious role in the divergence of mating cues that may influence species recognition, selection on reproductive characters may be an important source of more cryptic postmating barriers to cross-fertilization (Howard 1999) and even postzygotic hybrid breakdown (Adams 2005;Orr 2005). This is not surprising given the centrality of reproduction to the definition of species: traits and genes that affect interactions between males and females within populations are likely be among the first to cause reproductive incompatibilities between incipient species.…”