Life Cycle Evolution: From Simple Origins to Complex Adaptations and the Enigma of Senescence

The life cycle has been called the central unit in biology. In this chapter the origin and attributes of life cycles in general are discussed, and two of the many ecological questions are explored: why complex cycles as opposed to simple cycles have evolved, and whether all organisms are doomed to undergo senescence.

The inception of the life cycle is traceable to the simple cell cycle of prokaryotes. With the origin of multicellularity and eukaryote sex, life cycles became more expansive and identified with distinct phases related to developmental stage or nuclear condition. Apparently all organisms ultimately pass through a single-cell stage, which is advantageous in many ways: as a tabula rasa for implementing developmental novelties; in purging mutations from loaded individuals; and in aligning sub-organismal levels of selection.

When offspring are born into essentially the same habitat as the adults and do not undergo sudden ontogenetic change, the organism is said to have a simple life cycle (e.g., mammals). Where organisms have two or more ecologically distinct phases separated by an abrupt ontogenetic change, the life cycle is considered complex in ecological semantics (e.g., the frog, many species of which metamorphose from a tadpole living in a pond to an adult living on land. Other examples include toads, the holometabolous insects [i.e., those having a complete metamorphosis], various animal and plant parasites, and algae). An adaptive interpretation of the complex life cycle is that it appears to be (or at least to have been at the many points in geological time when it evolved) a specialization that allows the organism to exploit certain opportunities, and forgo compromises. Organisms with such cycles are adapted for particular activities such as feeding or reproduction in a particular stage.

The rust fungi, many of whose parasitic life cycles consist of a sequence of five morphological states on two distinct hosts, illustrate the intricacies and principles of the complex life cycle. CLCs in general and the rust cycle in particular usually have been interpreted adaptively. That reasoning follows in the rusts in part because of the seeming ideal match between pathogen stage and environment, and the truncation of the cycle in short-season environments somewhat analogous to progenesis (precocious sexual maturity in animals). However, the CLC may be an evolutionary dead-end and a prime example of how evolution can drive organisms to greater degrees of specialization.

In the rust case, the driving force would be an ever-deepening spiral of host-parasite coevolution. CLCs present a paradox because in theory they should be unstable over evolutionary time but have remained fixed in major taxa, including the rusts, even over geological time. Thus, an alternative interpretation of the CLC is that it persists 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.

Senescence is the manifestation of various deteriorative effects that decrease fecundity and the probability of survival with increasing age. It has been depicted most clearly at the population level by actuarial statistics showing an increasing mortality rate over time. If mortality is constant with age, the number of survivors declines exponentially and there is no basis for inferring from the data that senescence occurs. Non-senescent curves mean either that the organism inherently does not senesce or possibly that insufficient numbers of the population in nature pass through early- to mid-life for senescent effects to be detectable numerically.

Among macro organisms that reproduce largely or exclusively sexually, particularly the unitary organisms, a good case can be made for the occurrence of senescence. Examples include the vertebrates and many invertebrates such as the nematodes, crustaceans, insects as well as some plants such as the determinate annuals. On the other hand, evidence for senescence appears limited or nonexistent generally for modular organisms, including benthic sessile invertebrates, most perennial plants, and microorganisms. Indeed, there is evidence for some organisms that the probability of survival actually increases, along with fecundity, later in life. The terms ‘negligible senescence’ and ‘negative senescence’ have been used to describe such population dynamics.

The ultimate demise of clonal organisms, particularly clones of bacteria and fungi, is speculative. As genetic individuals, they can clearly be exceptionally long lived and of indeterminate size and duration, but there are virtually no actuarial statistics on the age-specific mortality or fecundity for such clones. Terms such as ‘immortality’ and ‘potential immortality’ are better suited to abstract mathematics, metaphysics, and religion than as biological descriptors in the senescence literature.

Senescence probably results mechanistically from multiple causation. In vertebrates and particularly in humans, these include decline of the immune and key organ systems leading to numerous forms of dysfunction manifested in diseases such as arthritis, neurological degeneration, cancer, and cardiovascular impairment. Among the specific causal factors implicated are faulty DNA repair, inflammation, crosslinking of macromolecules, and oxidative injury. Such progressive deterioration is attributable in part to cumulative insult and in part to defective repair. In an evolutionary context and as a first approximation, senescence is predicted to occur wherever the reproductive value of the individual diminishes with increasing age.

Thus, a gene with positive effects early in the reproductive period, that is, when reproductive value is high, will tend to be selected even if it may later have deleterious effects. Likewise, because of the declining strength of selection with age, pressure to remove harmful genes that are expressed late in life would be lower than for those acting early. The major evolutionary postulates relating to mutation accumulation, antagonistic pleiotropy, and a disposable soma are intuitive though backed up by relatively little convincing data. It remains generally unclear whether ‘senescence’ effects documented at the cellular level typically in research models are the cause or consequence of senescence at the organism level; likewise it is not clear or even likely that results from a few model organisms can be extrapolated to other taxa.

The occurrence of senescence among unitary organisms and its general absence or exceptionally delayed expression at the level of the genet among modular organisms is yet one more manifestation of the marked ecological difference between these two major groups of life forms. Most of the population dynamics and evolutionary theory have been developed for unitary organisms. Much remains to be done in sorting out the distinctive behaviors of these two classes and the biological research needed transcends the domain of microbiologists, botanists, or zoologists.