Hereditary stability and variation in evolution and development

Abstract

SUMMARY Evolution and development are both lineage processes but are often conceptualized as occurring by different and mutually exclusive mechanisms. It is conventionally asserted that evolution occurs via the random generation of diversity and the subsequent survival of those that pass selection. On the other hand, development is too often presented as proceeding via the unfolding of a deterministic program encoded in the DNA sequence. In biology, universal generalizations are rare and dogmas are often wrong for particular cases. Deterministic mechanisms contribute some of the new DNA sequences that subsequently become substrates for natural selection. Conversely, stochastic and selective mechanisms are intrinsic to development, and also to maintenance of the immune, and possibly, nervous systems. Cancer appears to be another process that straddles distinctions between evolutionary and developmental modes of hereditary change and stabilization. DNA sequence changes are an essential feature of many cancers, but there are also aspects of the disease similar to developmental lineage gone awry. The literature suggests that the cellular changes that give rise to cancer occur by mechanisms commonly associated with both evolutionary and developmental lineage pathways.

Positive selection in the evolution of cancer

“…Boström et al, 2000 ;Naora et al, 2001 ;Miller et al, 2003 a, b). These links between positive selection and cancer for HOX genes fit with Graham's (1992) hypothesis that rapid morphological evolution increases cancer risk (see also Thaler, 1999 ;Kavanagh, 2003;Leroi et al, 2003). We hypothesize that positively-selected HOX genes will also show evidence of pleiotropic effects on morphogenesis and cancer risk, or antagonistic coevolution, upon further study.…”

Evolutionary biology of cancer

“…Thus, pediatric cancers are rare, apparently as a result of their strongly negative fitness effects, but they are concentrated in two tissues, brain and bone, that have undergone striking recent evolutionary increases in size and growth trajectories along the human lineage. Such effects might have arisen as a byproduct of rapid shifts in the rate and timing of cell proliferation systems [42,43]. Similarly, a third tissue with high pediatric cancer rates, white blood cells, is subject to the effects of strong selection from host-parasite coevolution [41].…”

“…Several recent studies have provided evidence that, in reducing cancer risks, natural selection generates macroevolutionary constraints on morphology and development [40][41][42][43]. For example, a variant number of cervical vertebrae are strongly linked to pediatric cancer in humans, and the number of cervical vertebrae is highly conserved among most mammals [66].…”

The concept of developmental reprogramming and the quest for an inclusive theory of evolutionary mechanisms

“…The term "reprogramming" should not be interpreted as meaning that the developmental process and the structures to which it gives rise are precisely determined by the genes. In some cases, it may be best to view a mutation as shifting a series of probabilities of several structural variants (see review by Thaler 1999), rather than a phenomenon that causes an all-or-nothing switch from one variant structure to another. Also, in many cases environmental factors play a role in determining the pathway and outcome of development.…”