The long wait for hybrid sterility in flowering plants.

Related allopatric or parapatric speciesmay interbreedwhenhabitat 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 theproductionof homoploidhybrid derivatives (Hewitt, 2004; Arnold, 2006; Jaramillo-Correa et al., 2009; Soltis & Soltis, 2009). Even if hybrids are largely sterile, cross-breeding species may still generate allopolyploids. The lower the degree of fertility, the greater is the rate of unreduced gamete formation (Ramsey & Schemske, 1998). The window of opportunity for hybridization is finite. As lineages diverge, the potential for gene exchange or genetic union declines, because genomes become increasingly incompatible, that is, they accrue Dobzhansky–Muller (DM) incompatibilities (Coyne & Orr, 2004). As a consequence, the fertility of hybrids in plants typically declines as we go from intrataxon crosses, to crosses between races or subspecies, to crosses between closely related species, and to crosses between more distantly related ones (Levin, 1978; 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&Orr, 2004), but they are not substitutes for real time. The waiting time for hybrid sterility is a little-discussed metric in the plant literature, because amethod for itsmeasurement has not been forthcoming. We would like to know the approximate number of yr that two lineages can potentially influence each other’s gene pool or form allopolyploids.Moreover, we would like to know how long it takes to achieve a major milestone of allopatric speciation. Whereas we appreciate that ecological speciation may be relatively rapid, how much slower is the tempo of allopatric speciation? I propose that insights into this waiting time can be gained by relating the fertility of first-generation hybrids to estimates of the divergence times of species. The species considered will be the same ploidal level. Before applying this approach, it is important to recognize some of its limitations. First, data on hybrid fertility are available for few species employed in molecular phylogenetic studies. The small number of genes used in estimating divergence time may not be representative of the genome as a whole, in some instances residing in the nucleus and others in the cytoplasm, and may deviate from molecular rate constancy across lineages (Gaut et al., 2011). If species have exchanged genes, divergence time estimates may be substantially smaller than the actual time, especially if gene flow has been recent; 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 studiesmay 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 & Phillips, 2009; Schwartz & Mueller, 2010). In spite of the imperfection of relating hybrid fertility to divergence time estimates, we can gain a rough approximation of thewaiting times for partial hybrid sterility in several plant lineages, recognizing that time has probably been underestimated, perhaps substantially. The greater the amount of interspecific gene exchange that has taken place, the more the time to sterility will be underestimated. The approximate waiting time has value because it provides temporal insight into an important evolutionary process associated with speciation; and we did not have this before. As noted by Rieseberg & Willis (2007), ‘We know surprisingly little about the speed of plant speciation. ’ The approach taken here complements mathematical models that focus on how long it takes for lineages to develop postzygotic isolation as a result of DM incompatibilities. This time varies over orders of magnitude depending on model parameters (Gavrilets, 2000). I will show that, even erring on the conservative side, the waiting time for partial hybrid sterility is considerable. The onset of substantial fertility loss seems to be fairly consistent across several lineages, thus providing ameasure of confidence to the conclusions. The genera discussed in the following were all I could find after an exhaustive literature search. No genus or species combination was omitted because the time of fertility decline was inconsistent with others.