The developmental constraint interpretation

The constraint hypothesis emphasized by developmental biologists (see Moran 1994; Chap. 9 in Raff 1996) interprets CLCs as persisting because the stages are inherent parts of a developmental program largely beyond the reach of natural selection. Because of linkage among traits, modification of a stage may be restricted or precluded without adverse impact on others. Moran (1988) reviews the evidence for aphids that switch hosts.

She concludes that the cycle represents a historical constraint, being an evolutionary dead-end rather than a beneficial adaptation to optimize resource use. For such aphids, according to Moran, host alternation is a relict, maintained because a particular aphid morph (the fundatrix) became ‘over-specialized’ to the ancestral (woody) host, precluding the cycle moving in its entirety to the herbaceous host. In this case sequential specialization may be a trait difficult to jettison.

But, what of the rusts? Clearly many species have shown evolutionary plasticity in eliminating the alternate host and in some cases adopting a sharply abbreviated cycle in some populations but not in others (as in arctic vs. temperate latitudes, for example). As such they appear to be more malleable than do the aphids. Actually, some aphids evidently are more malleable than assumed by Moran and the adaptiveness of the CLC may be lineage-specific (Hardy et al. 2015). Have the rusts become too specialized?

Do they exemplify Harper’s (1982) observation that, far from representing the perfect match between organism and environment, partners in a coevolutionary spiral may drive each other into “ever deepening ruts of specialization”? (see also 7Chap. 3 and Huffaker 1964). Coevolutionary specialists do not necessarily endure such fates and a march from generalist to specialist is not supported by the broad phylogeny of specialization (Chap. 4 in Thompson 1994), ... “nor is there any reason to expect that specialization is an evolutionary dead end from which species cannot escape, or that specialists, as a rule, show sustained phylogenetic tracking of host taxa” (Thompson 1994, p. 75).

Overall, the complexities of CLCs, at least among parasites, are probably best interpreted in a situation-specific manner reflecting both constraint and natural selection: constraint on the life histories that lead to host alternation; on the adaptive elimination of a host after it has become a part of the life cycle; how that host is used in the relationship; and selection pressure for retention (Chap. 6 in Thompson 1994).