From molecules to ecology and back: the hierarchy theory view of speciation

Hierarchy theory (e.g. Salthe 1985, Eldredge 1986) provides a unifying approach for representing the multi-level structure of the organic world and an explanatory framework for the wide range of natural phenomena. Its birthdate can be located in the 1980s, when evolutionary biologists began exploring in detail the nature of hierarchical systems as an approach to understanding both the nature of these complex systems, and the nature of their interactions that underlie the evolutionary process. Nowadays hierarchy theory is being developed and updated in light of an explosion of new discoveries and fields, but also as a way of re-thinking and re-framing concepts, like speciation, that have been present in evolutionary theory for many decades. According to hierarchy theory, organisms are parts of at least two different kinds of systems: (1) matter-energy transfer systems, where organisms are parts of local populations that in turn are parts of local ecosystems. The economic roles played by such populations are what constitute ecological niches. Local ecosystems are parts of regional systems, a geographic mosaic of matter-energy transfer systems that together constitute the global biosphere. (2) genetically-based information systems: organisms are parts of local breeding populations that in turn are parts of each individual species. Species, through the process of evolution, are parts of historical lineages: genera, then families, orders etc. of the Linnaean Hierarchy. While evolutionary theory has legitimately focused most on genetic processes and the formation of genetic lineages, evolution does not occur in a vacuum: specifically, it is what takes place inside matter-energy transfer systems that determines, in large measure, the patterns of stability and change in genetic systems that we call “evolution”. The “sloshing bucket theory of evolution” (Eldredge 2003) is an example of how theoretical hierarchy theory applies to the real world of biological systems and their histories. The theory describes the multilevel interplay between ecological disruption, taxic extinction and consequent bursts of evolutionary diversification. The pulse, pace and scope of ecological disruptions – ranging from localized disturbances; regional, longer term disruptions; and (rarely) drastic global environmental change – have corresponding effects on dynamic matter-energy systems on different scales. Localized disruptions result in re-establishment of very similar local ecosystems, based on genetic recruitment of members of the same species still living outside the affected area; on the grandest scale, mass extinctions resulting from global environmental disruption witness the disappearance of larger-scale taxonomic entities. Over periods of millions of years (5-10 my, typically), the ecological roles played in the now-disrupted ecosystems by organisms in now-extinct groups are assumed by evolutionarily modified species that are derived from taxa that survived the extinction event. The intermediate situation – where regional ecosystems are disturbed, resulting in the extinction of many species – is perhaps of the greatest interest: the fossil record shows clearly that most speciation events (hence most evolutionary genetic change in the history of life) take place as a consequence of regional ecosystemic collapse and multiple extinctions of species across different lineages. Traditional presentations of speciation commonly depict one species at a time, and classify speciation events on a geographical basis (allopatric, peripatric, sympatric etc.). In light of hierarchy theory, both these habits are wrong, and a rethinking the process of speciation is needed to explicitly describe the interaction between (1) economic and (2) genealogical events. First, with “geographic speciation”, more than an eco-geographical event we actually mean one of the possible genealogical consequences of ecological barriers, i.e. the multiplication of genealogical entities at the level of species within instances of the evolutionary hierarchy (we use the biological concept of species, with no necessary link with the individuality thesis). As Gavrilets (2010) pointed out, a geographical taxonomy of speciation is silent about what happens in the genealogical hierarchy, for example about the kinds of genetic, morphological or behavioral “uncoordination” that yield reproductive isolation. A new taxonomy of processes of genealogical diversification (e.g., sympatric speciation, birth of varieties and subspecies, agamospecies) is possible. On the other hand, geographic barriers impact many species at once: ecological events which arguably trigger speciation are cross-phyletic. Second, a proper re-description of geographic speciation should contextualize the phenomenon properly in the scenario of ecological systems (ecosystems and, at a macroevolutionary time scale, faunas). Sometimes speciation can be adaptive (a critical assessment of its relative frequency would be necessary). But the important thing is that adaptation – usually seen from an intra-populational point of view – should as well be described in the context of ecological reassortment and reshaping of communities. We are in presence of contemporaneous processes that occur at the population-ecological time scale at different levels of the ecological hierarchy, inviting reinterpretation of the concepts of adaptation and fitness, coevolution, and niche construction. Intra-populational, inter-individual variation of ecologically relevant traits is examined as the “raw recruit” for natural selection. Transversal comparison among ecological communities brings into focus patterns in ecological processes and systems, and also processes like adaptive convergence. In this way, some epistemological problems which are usually related to adaptation disappear, and new ways of framing the issue emerge. For example, coevolution is not a separate issue, neither it is niche construction, i.e., the cross-genealogical modification of selective pressures as a consequence of the existence and activity of populations, including the interactive role of abiotic factors. It is important to remark that this re-worked speciation concepts seems to play a key role in the most updated views on hominid evolution.