The biotic crisis and the future of evolution

The Core Concept

One of the first truisms absorbed by biologists is that evolution is not predictable. We can no more predict the future composition of communities than some Ordovician ecologist could have foreseen the Great Barrier Reef. However, despite our inability to predict the products of evolution—the trajectories of future morphologies or the innovations of future physiologies—we can make meaningful estimates about evolutionary processes as they will be affected by the depletion of biological diversity. We may have little basis for predicting what large mammals might look like two million years from now, but much better reason to suppose that there will be very few of them.

The evolutionary dimension to the current biotic crisis has been vividly expressed by Michael Soule (10): “Death is one thing, an end to birth is something else.” In other words, impending extinctions will be far from the full final outcome of current environmental disruption. At least as important will be the alteration of evolutionary process, and for a period that is difficult to estimate but must surely measure in millions of years.

Lessons from the Past?

The geological record is replete with extinction events, their intensity ranging from the small and local to global mass extinctions that shattered Earth's biological order. Inevitably, extinctions were followed by rediversification, directed in the case of the largest events by ecological reorganization. What can we learn from paleobiology, other than the oft-quoted observation that recovery proceeds slowly in the wake of grand scale biotic disruption (40, 53, 54)? Can we find generalities among extinction episodes that can guide thinking about our own future? Or, is it the differences among extinction events that should command our attention? As David Jablonski (63) asks in these proceedings, should we even focus on the five great mass extinctions that capture most attention, or do the more numerous, smaller events scattered throughout the geological record provide closer analogs for the present?

The geologic record contains much evidence of bounce-back processes (49, 54–59), but how far will these serve as analytic blueprints for what lies ahead? How can we estimate time frames at issue? Should we anticipate a minimum period of several million years [perhaps as much as 10 million (56)] before evolution can reestablish anywhere near the biological configurations and ecological circuitry existing before the current crisis? Will some recovery processes operate in some sectors of the biosphere, others in others, and with widely varying rates (55, 58, 60)?

In some major extinctions, for example the Cretaceous-Tertiary boundary event, environmental perturbation was swift and sure, but also short-lived. Recovery began soon after disruption. In the present biotic crisis, it is hard to envision a scenario under which the factors that are driving the biosphere toward grand scale biodiversity loss will be mitigated in the wake of such loss. On the contrary, on any time scale we can envisage (and any scenario that does not involve early mass mortality for humankind), the situation becomes bad and then stays bad for some time to come. Thus, on the time scale of the human species, environmental disruption (or at least aspects of it) is permanent. Under these circumstances (which may, to some degree, be approximated by the persistent environmental discord after the Permian-Triassic mass extinction), the prospects for rediversification are limited.

Recovery Processes

How will ecosystems function in a world of diminished biodiversity? Does ecosystem function necessarily decay as diversity declines, and if so, by how much and in what manner? Can biodiversity and humans alike prosper in a world where most biological diversity will be confined to relatively small parks and reserves?

If biodiversity is indeed critical to ecosystem function, do we know enough about the principles of evolution to intervene in the recovery processes? To the extent that the answer to the first part of this question is probably “yes” and the answer to the second part is almost certainly “no,” what would we need to learn to attempt evolutionary interventions that will do more good than harm?

More realistically, do we know enough to mitigate the loss of biological diversity? As David Western writes in his colloquium contribution, mitigating strategies will likely be carried out predominantly in ecosystems dominated or influenced by humans and other species that thrive when humans are present. How we think about our evolutionary future depends directly on how successful we can hope to be in preserving biodiversity and biodisparity.

Which taxa are likely to play prominent parts in recovery processes? What “survivorship” traits (ecological, biogeographic, evolutionary) can we use to define those taxa that may prove more successful in surviving current events? At the same time, which taxa might [to cite Erwin's graphic phrase (55)] “win the extinction but lose the recovery?” Might certain biotas already be “stressed” by Pleistocene climatic oscillations, making them more vulnerable to depletion (61, 62)? Or are they “hardened”—purged of their most vulnerable members by Pleistocene events (63)?

Should we in fact speak of “recovery”? What is it that is supposed to be recovering (the dinosaurs didn't)? Should we not view the recovery phase as more like a transition to new and novel departures of multiple sorts (55)? Plainly there is much scope for pioneering research in response to the many questions raised (54). We need to consider planning priorities. What research is most pressing? What is readily achievable? What is already underway? What deserves most financial or institutional support? What potential is there for interdisciplinary research, for instance that which combines genetics and restoration ecology, or paleontology and conservation biology?

Conservation Responses

Should we be content simply to safeguard as much as we can of the planetary stock of species? Or should we pay equal if not greater attention to safeguarding evolutionary processes at risk (cf. refs. 64–66)? Consider, for instance, biodisparity: to cite Jablonski (49), “If we are concerned with avoiding the loss of particular functional groups, or with maximizing the potential source pool for evolutionary recovery, then biodisparity measures may provide a more appropriate assessment, beyond sheer numbers of taxa, of how priorities should be set.”

Following on from these considerations is the question of whether we should seek to maintain the evolutionary status quo by preserving precise phenotypes of particular species, or whether we should prefer to maintain phylogenetic lines that will enable evolutionary adaptations to persist, thereby leading to new species (67, 68). Is it sufficient for us to maintain, for example, just the two elephant species we already have, or should we try to keep open the evolutionary option of further elephant-like species in the distant future?

This is an unusually significant question, with unusually significant implications for conservation strategies. Elephants, along with many other large mammals, are inclined to move around a good deal, a trait that enables them to maintain gene flow across large areas. As a result, their gene pools often tend to be fairly uniform [an elephant in East Africa may not be so different from one 4,000 km away in South Africa (68)]. Regrettably the remaining populations of elephants, substantial and extensive as they are, albeit fragmented and declining fast, are probably already below the minimum numbers to keep open the possibility of speciation (69).

In marked contrast to elephants, with their slow breeding rates, many insect species have immense breeding capacities and rapid turnover rates. These latter attributes offer quick adaptability to environmental shifts, whereupon genetic changes are passed along promptly. These attributes not only leave many insect species well suited to survive the environmental upheavals of human activities, but they offer exceptional scope for speciation in comparatively short order. By contrast, elephants, together with other large-bodied species that reproduce slowly and hence possess restricted capacity for genetic adaptation, will be at an extreme evolutionary disadvantage. Does this factor imply that they should therefore receive all of the greater attention from conservationists—or that, in a triage situation, they should rank lower in our priorities? Although this is a fundamental question, it has hardly been addressed.

An even more important consideration arises concerning those origination centers and radiation lineages that serve as “evolutionary fronts” (67). From the standpoint of future evolution, it is surely more appropriate to safeguard the main potential for diversity generation than to emphasize the primary focus of many current conservation programs, viz. individual taxa and, especially, endemic taxa (70, 71). Much the same applies with respect to those functional groups that increase the potential for evolutionary recovery (49).

All in all, the prospect is that, in the wake of the present biodiversity crisis, we shall find that many evolutionary processes that have persisted throughout the Phanerozoic Eon will be slowed if not depauperized for an extended period. This is not to say, of course, that evolution will come to a halt, or even that speciation will be suspended (except for the large vertebrates). In fact, there may be enough creative disruption in certain environments to foster some extremely rapid microevolutionary changes, attended by (localized?) bursts of speciation. But there will surely be reduced scope for speciation on the scale that has characterized the past many millions of years.

These, then, are some of the issues that we should bear in mind as we begin to impose a fundamental shift on evolution's course. We are “deciding” on evolution's future in virtually a scientific vacuum—deciding all too unwittingly, but effectively and increasingly. Hence the importance of the Colloquium's findings as set out in this special issue of PNAS.