Optimization and Constraint in Molding Life Cycles

The CLC has been explained in terms of both adaptation and developmental constraint (Moran 1994; Chap. 9 in Raff 1996). According to the former, it has arisen and is maintained as a means of accommodating the conflicting needs of competitive growth at a fixed site or time with genetic exchange and dispersal of offspring to new sites or to better conditions at a later time. According to the latter, it is a developmental constraint, nothing more than a historical legacy, retained because there is no alternative ontogenetic pathway.

The adaptive interpretation The CLC allows important activities to be segregated by specialized stage, the organism moving progressively from one functional compartment into another, broadly speaking by metamorphosis. In this manner it can exploit transient opportunities (Wilbur 1980), efficiently executing one task rather than compromising among many as do organisms with a SLC. As we have seen in the multigenerational type of CLC typified by the rusts, the uredinium and its associated spores evolved as the long-range, repeating, dispersal stage; the spermogonium is specialized for nuclear transfer and fertilization; and the telium is the main resistant (overwintering) stage associated with survival and karyogamy. Fleeting opportunities—for example, in the form of an accessible alternate host at precisely the appropriate stage of susceptibility and in an environment conducive for infection—are clearly just as apparent for parasites with CLCs as they are for, say, anuran larvae in resource- rich but temporary ponds, or insect larvae that feed on carrion or seeds.

It is apparent that where a CLC includes heteroecy, host shifting has usually been interpreted as currently adaptive. Because organisms with CLCs exhibit ‘decoupling’ or compartmentation of stages, the opportunity arises for independent evolution in the different phases. The extent to which this may occur is contested (Istock 1967; Strathmann 1974; Bonner 1982b, pp. 226-229; Petranka 2007). Based on a life table model, Istock (1967) proposed that the adaptiveness of the two stages of a hypothetical organism with a larval and an adult form is largely independent. He suggested further that it is this independence that usually makes CLCs unstable over evolutionary time because the flow rates of individuals between the phases are unbalanced (e.g., flow of larvae from the larval to the adult environment; flow of progeny from the adult to the larval environment).

In Istocks CLC model, the ecological advantages are fully exploited only where both the larval and adult compartments are demographically saturated (Istock 1967). Even if achieved in nature, he notes that this condition is very difficult to maintain over evolutionary time, leading eventually to reduction or loss of one of the stages. Strathmann (1974), on the other hand, using marine invertebrates as an example, emphasized that evolutionary feedback acts in regulatory fashion to integrate the various phases. Interaction between the two phases is described for marine intertidal invertebrates by Roughgarden et al. (1988).

In the microbial context, it would be interesting to know to what extent the various stages (such as the oversummering parasitic phase in contrast to the overwintering, saprophytic phase) in plant pathogen life cycles can be modified independently or whether there is close overall evolutionary coordination. (This is roughly analogous to the cycle of a songbird that spends its summers in Canada or the northern U.S. and winters in the Caribbean or Mexico, adjusting to the markedly different habitat in each place.) In other words, how plastic is the overall life cycle? Regarding the rusts in particular, evolution of the CLC and particularly host alternation arguably was one mechanism whereby certain fungal parasites were able to advance from their early hosts, possibly in the primeval swamp, into otherwise inhospitable environments represented in part by new host taxa. As noted earlier, the extraordinary complexity of the rust cycle is unique; if assessed on its prevalence among taxa, it must therefore be judged a relatively unsuccessful evolutionary experiment. Nevertheless, the rusts persist, just as do the amphibians with their CLC.