The long wait for hybrid sterility in flowering plants

Related allopatric or parapatric species may interbreed when habitat disturbance, long-distance dispersal, and environment-mediated range shifts allow species contact. Correlatively, ecologically isolated sympatric species may hybridize following environmental/habitat alteration. If hybrids are fertile, such contact could lead to extensive introgression or to the production of homoploid hybrid derivatives (Hewitt, 2004; Arnold, 2006; Jaramillo-Correa et al., 2009; Soltis Grant, 1981; Rieseberg et al., 2006). Correlatively, the ability to make fertile hybrids also declines with increasing genetic distance in plants (Moyle et al., 2004; Scopece et al., 2007, 2008). What is causal in this relationship remains to be determined. Allozyme distance has been widely used as a surrogate for evolutionary time, as have DNA-based measures (Edmands, 2002; Coyne and gene exchange may occur even if hybrid fertility is low (Strasburg et al., 2009; Sambatti et al., 2012). If the fertility relationships of two species vary among their populations (Levin, 1978; Grant, 1981), and if there are barriers to gene flow among conspecific populations (Scopece et al., 2010), then the few populations chosen for hybridization and divergence time studies may not be representative of the species as a whole. To the extent that hybrid fertility decline is the result of chromosomal rearrangement, lineages may differ in their penchant for rearrangement, which may occur relatively quickly (Levin, 2002). Finally, the approach used in this paper is restricted by the considerable error terms in phylogenetic estimates of divergence times (Ho Schwartz and we did not have this before. As noted by Rieseberg Carr, 1995). The genus Draba provides an exception to the slow pace of fertility decline (Grundt et al., 2006). Low degrees of genetic differentiation within and among Draba nivalis, Draba subcapitata, and Draba fladnizensis suggest that each species probably originated within the past 1 million yr. Yet progeny of crosses within regions among populations of D. fladnizensis were semisterile, and crosses among proximal D. nivalis populations were mostly sterile. Crosses among regions within the three species were largely sterile. The observed correlation between hybrid sterility and genetic distance implies that this postzygotic barrier accrues in a gradual (stepwise) manner. In D. nivalis, reduced interpopulation fertility is attributable in part to underdominant chromosomal rearrangements and in part to DM incompatibilities (Skrede et al., 2008). Genetic drift in these predominantly self-fertilizing species is the most likely explanation for the relatively rapid bloom of hybrid sterility (Grundt et al., 2006; Skrede et al., 2008). The establishment of underdominant mutations by genetic drift, as promoted by small effective population size, and by cycles of localized extinction and recolonization (Lande, 1985; Gavrilets, 2004), fosters the formation of cryptic species as seen in Draba and elsewhere (Grant, 1981). As noted, hybrid sterility may have multiple causes. Genetic incompatibility contributes to the sterility of hybrids in many genera (e.g. Mimulus, Fishman Solanum, Moyle Oryza, Li et al., 2008). Indeed, an association between the levels of pairing anomalies and sterility in hybrids does not necessarily indicate that the anomalies are the prime cause of sterility (Lowry et al., 2008). Conversely, pairing anomalies do seem to explain sterility in the silversword alliance (Carr Carr, 1995), and the recovery of fertility in polyploid derivatives of sterile hybrids indicates that DM incompatibilities were not responsible for those instances of hybrid sterility (Rieseberg Renner et al., 2008). The longer waiting time for sterility in trees than in herbs is not surprising, since the generation time in trees is much longer than that in herbs. Notably, the rate of molecular evolution in herbaceous plants is roughly 2.5 times faster than in woody plants based on a global phylogenetic analysis of angiosperms (Smith Givnish, 2010), whereas hybrid sterility is thought to build through the gradual stochastic accumulation of many DM incompatibilities with small effects (Orr Coyne Seehausen, 2002; Mendelson, 2003; Fitzpatrick, 2004; Malone Price Keeley et al., 2011). In general, chromosomal evolution in the Hawaiian flora has been rather muted (Stuessy et al., 1998). It is likely that many lineages evolve prezygotic barriers, but expire before the appearance of postzygotic barriers (Rosenblum et al., 2012). In contrast to hybrid sterility, the degree of prepollination isolation does not progressively increase over time, because the niches of related lineages do not progressively diverge over time (Prinzing et al., 2001; Wiens Couvreur et al., 2011; Peterson, 2011). Once established, the niches of related species tend to be relatively constant, being conserved by habitat selection, pleiotropy, and interpopulation gene flow, and the lack of genetic variation that might allow a niche shift (Wiens, 2004). Accordingly, when prezygotic barriers are breached or when species migrate long distances naturally or with the aid of humans, hybridization may occur between taxa long separated in the same or distant regions (Abbott et al., 2003). The fact that herbaceous species that diverged 3–4 mya (or much longer in the case of trees) may retain the potential to exchange genetic material has important ramifications. First, the long time to hybrid sterility means that the patterns of genetic variation within contemporary species may have been shaped by numerous episodes of gene exchange with sister taxa at many times in the near and deep past. Whereas discussions of ancient hybridizations often focus on Holocene expansions from glacial refugia (e.g. Hewitt, 2004; Petit et al., 2004; Jaramillo-Correa et al., 2009), the gene pools of contemporary species (especially trees) may reflect much earlier and potentially repeated exchanges of genetic material. Secondly, there is a very long period during which substantive gene exchange may have led to the fusion of incipient species or to the retardation of species divergence (Seehausen et al., 2008; Gilman & Behm, 2011). Correlatively, there is a very large window of time during which a given taxon pair may have spawned hybrid species. The accrual of chromosome pairing abnormalities (and attendant fertility reduction) in hybrids increases the production of unreduced gametes, and thus the likelihood of allopolyploid formation (Ramsey & Schemske, 1998). The notion of a very slow development of hybrid sterility is consistent with the observation that millions of yr have transpired between the split of two lineages and the origin of their allopolyploids. Consider that the B and C genomes of the Oryza officinalis complex split c. 4 mya, but tetraploids formed only between 0.3 and 0.6 mya (Wang et al., 2009). The lineages of Brassica oleracea and Brassica rapa diverged roughly 3.7 mya, whereas its allotetraploid derivative Brassica napus arose < 10 000 yr ago (Cheung et al., 2009). The progenitors of Nicotiana tabacum diverged c. 4.5 mya, whereas the latter arose only 0.2 mya (Clarkson et al., 2005). In these and other cases, the long time to allopolyploid formation may reflect a long wait for progenitor sympatry, as well as for reduced hybrid fertility. We would hope to gain information that would provide a better understanding of the hybrid sterility dynamic. Divergence time estimates that were based on multiple markers, and on multiple populations of two species, would be most informative, as would hybrid fertility rates from the same multiple populations. If divergence times could be estimated for some populations that were allopatric and others that were sympatric with the related species, we might observe the effect of recent interspecific gene exchange (divergence time estimates would be reduced). This paper is the first attempt at bringing a temporal perspective to the development of a postpollination barrier between species sharing the same ploidal level. In doing so, it brings us closer to understanding the tempo of allopatric speciation. In addition to better documenting fertility descent in time, it behoves us to consider the pace at which species crossability and hybrid viability decline, as they too are products of genomic dissonance. With the speed of barrier building in hand, we will finally appreciate the time required for two gene pools to become incompatible in all respects. The author is grateful to Richard Abbott, Sally Otto, and three anonymous reviewers for their thoughtful critiques of the paper.