Oppositions in panbiogeography: Can the conflicts between selection,constraint, ecology,and history be resolved?

Abstract

Croizat’s radical attack on traditional modes of biological inquiry has produced strongly polarised responses. Instead of arguing for or against the panbiogeographic approach I attempt to analyse some basic assumptions shared by both its defenders and critics. Although their emphasis is quite different both sides rely on two central oppositions. In evolutionary arguments selective explanations are opposed to those emphasising phylogenetic constraint (orthogenesis). In biogeographic arguments ecological explanations are opposed to historical explanations. I discuss how the legendary opposition between nature and nurture was resolved by reformulating the way in which causation was viewed. I suggest that the selection/constraint opposition shares many features in common with the nature/nurture opposition and argue that it can be resolved in a similar manner. Conflicts between ecological and historical explanations in biogeography are explored by contrasting Diamond’s analysis of New Guinea bird distributions with that of Croizat’s. By again drawing on the resolution of the nature/nurture dispute a way of synthesising ecological and historical explanations is outlined.     

Origin of the fittest: link between emergent variation and evolutionary change as a critical question in evolutionary biology

In complex organisms, neutral evolution of genomic architecture, associated compensatory interactions in protein networks and emergent developmental processes can delineate the directions of evolutionary change, including the opportunity for natural selection. These effects are reflected in the evolution of developmental programmes that link genomic architecture with a corresponding functioning phenotype. Two recent findings call for closer examination of the rules by which these links are constructed. First is the realization that high dimensionality of genotypes and emergent properties of autonomous developmental processes (such as capacity for self-organization) result in the vast areas of fitness neutrality at both the phenotypic and genetic levels. Second is the ubiquity of context- and taxa-specific regulation of deeply conserved gene networks, such that exceptional phenotypic diversification coexists with remarkably conserved generative processes. Establishing the causal reciprocal links between ongoing neutral expansion of genomic architecture, emergent features of organisms' functionality, and often precisely adaptive phenotypic diversification therefore becomes an important goal of evolutionary biology and is the latest reincarnation of the search for a framework that links development, functioning and evolution of phenotypes. Here I examine, in the light of recent empirical advances, two evolutionary concepts that are central to this framework-natural selection and inheritance-the general rules by which they become associated with emergent developmental and homeostatic processes and the role that they play in descent with modification.     

Key evolutionary innovations and their ecological mechanisms

Explanations for taxonomic diversity in a particular clade often implicate evolutionary innovations, possessed by members of the clade, that are thought to have favoured diversification. We review such “key innovation”; hypotheses, the ecological mechanisms involved, and potential tests of such hypotheses.

Key innovation hypotheses can be supported by evidence of ecological mechanism and by comparative tests. We argue that both are necessary for convincing support. In fact, few key innovation hypotheses are currently backed by either one.

We group ecological mechanisms of diversification in three major classes. Diversification may be spurred by innovations that: I) allow invasion of new adaptive zones; II) increase fitness, allowing one clade to replace another; or III) increase the propensity for reproductive or ecological specialization. Key innovations in different classes are likely to produce different evolutionary patterns, and therefore may be supported by different kinds of ecological evidence.     

Oceanic island biogeography through the lens of the general dynamic model: assessment and prospect

The general dynamic model of oceanic island biogeography (GDM) has added a new dimension to theoretical island biogeography in recognizing that geological processes are key drivers of the evolutionary processes of diversification and extinction within remote islands. It provides a dynamic and essentially non‐equilibrium framework generating novel predictions for emergent diversity properties of oceanic islands and archipelagos. Its publication in 2008 coincided with, and spurred on, renewed attention to the dynamics of remote islands. We review progress, both in testing the GDM's predictions and in developing and enhancing ecological–evolutionary understanding of oceanic island systems through the lens of the GDM. In particular, we focus on four main themes: (i) macroecological tests using a space‐for‐time rationale; (ii) extensions of theory to islands following different patterns of ontogeny; (iii) the implications of GDM dynamics for lineage diversification and trait evolution; and (iv) the potential for downscaling GDM dynamics to local‐scale ecological patterns and processes within islands. We also consider the implications of the GDM for understanding patterns of non‐native species diversity. We demonstrate the vitality of the field of island biogeography by identifying a range of potentially productive lines for future research.     

Phylogentic constraints,adaptive syndromes,and emergent properties: From individuals to population dynamics

The hypothesis is developed that there are causal linkages in evolved insect herbivore life histories and behaviors from phylogenetic constraints to adaptive syndromes to the emergent properties involving ecological interactions and population dynamics. Thus the argument is developed that the evolutionary biology of a species predetermines its current ecology.Phylogenetic Constraints refer to old characters in the phylogeny of a species and a group of species which set limits on the range of life history patterns and behaviors that can evolve. For example, a sawfly is commonly limited to oviposition in soft plant tissue, while plants are growing rapidly.Adaptive Syndromes are evolutionary responses to the phylogenetic constraints that minimize the limitations and maximize larval performance. Such syndromes commonly involve details of female ovipositional behavior and how individuals make choices for oviposition sites relative to plant quality variation which maximize larval survival. Syndromes also involve larval adaptations to the kinds of choices females make in oviposition. The evolutionary biology involved with phylogenetic constraints and adaptive syndromes commonly predetermines the ecological interactions of a species and its population dynamics. Therefore, these ecological interactions are calledEmergent Properties because they are natural consequences of evolved morphology, behavior, and physiology. They commonly strongly influence the three-trophic-level interactions among host plants, insect herbivores, and carnivores, and the relative forces of bottom-up and top-down influences in food webs. The arguments are supported using such examples as galling sawflies and other gallers, shoot-boring moths and beetles, budworms, and forest Macrolepidoptera. The contrasts between outbreak or eruptive species and uncommon and rare species with latent population dynamics are emphasized.     

Units and passages: A view for evolutionary biology and ecology

Many authors, including paleobiologists, cladists and so on, adopt a nested hierarchical viewpoint to examine the relationships among different levels of biological organization. Furthermore, species are often considered to be unique entities in functioning evolutionary processes and one of the individuals forming a nested hierarchy.I have attempted to show that such a hierarchical view is inadequate in evolutionary biology. We should define units depending on what we are trying to explain. Units that play an important role in evolution and ecology do not necessarily form a nested hierarchy. Also the relationships among genealogies at different levels are not simply nested. I have attempted to distinguish the different characteristics of passages when they are used for different purposes of explanation. In my analysis, species and monophyletic taxa cannot be uniquely defined as single units that function in ecological and evolutionary processes.The view discussed in this paper may provide a more general basis for testing competing theories in evolution, and provide new insights for future empirical studies.     

Clonal architecture in marine macroalgae: ecological and evolutionary perspectives

The study of the ecological and evolutionary consequences of clonal growth in vascular plants has been widely addressed; however, marine macroalgae, which are interesting modular organisms that combine simple morphologies and complex life cycles, have been almost ignored. This paper presents a review and analysis of the ecological and evolutionary consequences of clonality in marine macroalgae, including three main subjects: (1) modular construction (modules and ramets); (2) life cycle and evolutionary perspectives, and (3) ecological perspectives of clonality in marine macroalge. The biological emergent attributes of clonality are present in marine macroalgae e.g. high longevity of the genet by the continual renewal of modules, and variable morphological plasticity of ramets and modules in relation to environmental conditions. However, experimental work is still needed to solve questions such as the effect of crowding on survival rates and use of resources, as well as its effect on sexual or asexual patterns of reproduction. I expect that the study of the evolutionary consequences of the combined presence of alternation of generations and clonal growth in marine macroalgae will make important contributions to clonal plant theory.     

Tri‐trophic interactions: bridging species,communities and ecosystems

A vast body of research demonstrates that many ecological and evolutionary processes can only be understood from a tri‐trophic viewpoint, that is, one that moves beyond the pairwise interactions of neighbouring trophic levels to consider the emergent features of interactions among multiple trophic levels. Despite its unifying potential, tri‐trophic research has been fragmented, following two distinct paths. One has focused on the population biology and evolutionary ecology of simple food chains of interacting species. The other has focused on bottom‐up and top‐down controls over the distribution of biomass across trophic levels and other ecosystem‐level variables. Here, we propose pathways to bridge these two long‐standing perspectives. We argue that an expanded theory of tri‐trophic interactions (TTIs) can unify our understanding of biological processes across scales and levels of organisation, ranging from species evolution and pairwise interactions to community structure and ecosystem function. To do so requires addressing how community structure and ecosystem function arise as emergent properties of component TTIs, and, in turn, how species traits and TTIs are shaped by the ecosystem processes and the abiotic environment in which they are embedded. We conclude that novel insights will come from applying tri‐trophic theory systematically across all levels of biological organisation.     

Emergent properties and the context objection to reduction

Reductionism is a central issue in the philosophy of biology. One common objection to reduction is that molecular explanation requires reference to higher-level properties, which I refer to as the context objection. I respond to this objection by arguing that a well-articulated notion of a mechanism and what I term mechanism extension enables one to accommodate the context-dependence of biological processes within a reductive explanation. The existence of emergent features in the context could be raised as an objection to the possibility of reduction via this strategy. I argue that this objection can be overcome by showing that there is no tenable argument for the existence of emergent properties that are not susceptible to a reductive explanation.     

Innovativeness as an emergent property: a new alignment of comparative and experimental research on animal innovation

Innovation and creativity are key defining features of human societies. As we face the global challenges of the twenty-first century, they are also facets upon which we must become increasingly reliant. But what makes Homo sapiens so innovative and where does our high innovation propensity come from? Comparative research on innovativeness in non-human animals allows us to peer back through evolutionary time and investigate the ecological factors that drove the evolution of innovativeness, whereas experimental research identifies and manipulates underpinning creative processes. In commenting on the present theme issue, I highlight the controversies that have typified this research field and show how a paradigmatic shift in our thinking about innovativeness will contribute to resolving these tensions. In the past decade, innovativeness has been considered by many as a trait, a direct product of cognition, and a direct target of selection. The evidence I review here suggests that innovativeness will be hereon viewed as one component, or even an emergent property of a larger array of traits, which have evolved to deal with environmental variation. I illustrate how research should capitalize on taxonomic diversity to unravel the full range of psychological processes that underpin innovativeness in non-human animals.     

Patterns and mechanisms of genetic and phenotypic differentiation in marine microbes

Microbes in the ocean dominate biogeochemical processes and are far more diverse than anticipated. Thus, in order to understand the ocean system, we need to delineate microbial populations with predictable ecological functions. Recent observations suggest that ocean communities comprise diverse groups of bacteria organized into genotypic (and phenotypic) clusters of closely related organisms. Although such patterns are similar to metazoan communities, the underlying mechanisms for microbial communities may differ substantially. Indeed, the potential among ocean microbes for vast population sizes, extensive migration and both homologous and illegitimate genetic recombinations, which are uncoupled from reproduction, challenges classical population models primarily developed for sexually reproducing animals. We examine possible mechanisms leading to the formation of genotypic clusters and consider alternative population genetic models for differentiation at individual loci as well as gene content at the level of whole genomes. We further suggest that ocean bacteria follow at least two different adaptive strategies, which constrain rates and bounds of evolutionary processes: the 'opportunitroph', exploiting spatially and temporally variable resources; and the passive oligotroph, efficiently using low nutrient concentrations. These ecological lifestyle differences may represent a fundamental divide with major consequences for growth and predation rates, genome evolution and population diversity, as emergent properties driving the division of labour within microbial communities.     

Measurement of the Girth of Coniferous Trees at Braemar in 1894

ABSTRACT

Background: Plant communities are usually characterised by species composition and abundance, but also underlie a multitude of complex interactions that we have only recently started unveiling. Yet, we are still far from understanding ecological and evolutionary processes shaping the network-level organisation of plant diversity, and to what extent these processes are specific to certain spatial scales or environments.

Aims: Understanding the systemic mechanisms of plant–plant network assembly and their consequences for diversity patterns.

Methods: We review recent methods and results of plant–plant networks.

Results: We synthetize how plant–plant networks can help us to: (a) assess how competition and facilitation may balance each other through the network; (b) analyse the role of plant–plant interactions beyond pairwise competition in structuring plant communities, and (c) forecast the ecological implications of complex species dependencies. We discuss pros and cons, assumptions and limitations of different approaches used for inferring plant–plant networks.

Conclusions: We propose novel opportunities for advancing plant ecology by using ecological networks that encompass different ecological levels and spatio-temporal scales, and incorporate more biological information. Embracing networks of interactions among plants can shed new light on mechanisms driving evolution and ecosystem functioning, helping us to mitigate diversity loss.     

Rapid evolution and the convergence of ecological and evolutionary time

Recent studies have documented rates of evolution of ecologically important phenotypes sufficiently fast that they have the potential to impact the outcome of ecological interactions while they are underway. Observations of this type go against accepted wisdom that ecological and evolutionary dynamics occur at very different time scales. While some authors have evaluated the rapidity of a measured evolutionary rate by comparing it to the overall distribution of measured evolutionary rates, we believe that ecologists are mainly interested in rapid evolution because of its potential to impinge on ecological processes. We therefore propose that rapid evolution be defined as a genetic change occurring rapidly enough to have a measurable impact on simultaneous ecological change. Using this definition we propose a framework for decomposing rates of ecological change into components driven by simultaneous evolutionary change and by change in a non‐evolutionary factor (e.g. density dependent population dynamics, abiotic environmental change). Evolution is judged to be rapid in this ecological context if its contribution to ecological change is large relative to the contribution of other factors. We provide a worked example of this approach based on a theoretical predator–prey interaction [ Abrams, P. & Matsuda, H. (1997) . Evolution, 51, 1740], and find that in this system the impact of prey evolution on predator per capita growth rate is 63% that of internal ecological dynamics. We then propose analytical methods for measuring these contributions in field situations, and apply them to two long‐term data sets for which suitable ecological and evolutionary data exist. For both data sets relatively high rates of evolutionary change have been found when measured as character change in standard deviations per generation (haldanes). For Darwin's finches evolving in response to fluctuating rainfall [ Grant, P.R. & Grant, B.R. (2002) . Science, 296, 707], we estimate that evolutionary change has been more rapid than ecological change by a factor of 2.2. For a population of freshwater copepods whose life history evolves in response to fluctuating fish predation [ Hairston, N.G. Jr & Dillon, T.A. (1990) . Evolution, 44, 1796], we find that evolutionary change has been about one quarter the rate of ecological change – less than in the finch example, but nevertheless substantial. These analyses support the view that in order to understand temporal dynamics in ecological processes it is critical to consider the extent to which the attributes of the system under investigation are simultaneously changing as a result of rapid evolution.     

Biogeographic responses and niche occupancy of microbial communities following long-term land-use change

Understanding the effects of forest-to-agriculture conversion on microbial diversity has been a major goal in soil ecological studies. However, linking community assembly to the ruling ecological processes at local and regional scales remains challenging. Here, we evaluated bacterial community assembly patterns and the ecological processes governing niche specialization in a gradient of geography, seasonality, and land-use change, totaling 324 soil samples, 43 habitat characteristics (abiotic factors), and 16 metabolic and co-occurrence patterns (biotic factors), in the Brazilian Atlantic Rainforest, a subtropical biome recognized as one the world’s largest and most threatened hotspots of biodiversity. Pairwise beta diversities were lower in pastures than in forest and no-till soils. Pasture communities showed a predominantly neutral model, regarding stochastic processes, with moderate dispersion, leading to biotic homogenization. Most no-till and forest microbial communities followed a niche-based model, with low rates of dispersal and weak homogenizing selection, indicating niche specialization or variable selection. Historical and evolutionary contingencies, as represented by soil type, season, and dispersal limitation were the main drivers of microbial assembly and processes at the local scale, markedly correlated with the occurrence of endemic microbes. Our results indicate that the patterns of assembly and their governing processes are dependent on the niche occupancy of the taxa evaluated (generalists or specialists). They are also more correlated with historical and evolutionary contingencies and the interactions among taxa (i.e., co-occurrence patterns) than the land-use change itself.

     

A conceptual framework of evolutionary novelty and innovation

Since 1990 the recognition of deep homologies among metazoan developmental processes and the spread of more mechanistic approaches to developmental biology have led to a resurgence of interest in evolutionary novelty and innovation. Other evolutionary biologists have proposed central roles for behaviour and phenotypic plasticity in generating the conditions for the construction of novel morphologies, or invoked the accessibility of new regions of vast sequence spaces. These approaches contrast with more traditional emphasis on the exploitation of ecological opportunities as the primary source of novelty. This definitional cornucopia reflects differing stress placed on three attributes of novelties: their radical nature, the generation of new taxa, and ecological and evolutionary impact. Such different emphasis has led to conflating four distinct issues: the origin of novel attributes (genes, developmental processes, phenotypic characters), new functions, higher clades and the ecological impact of new structures and functions. Here I distinguish novelty (the origin of new characters, deep character transformations, or new combinations) from innovation, the ecological and evolutionary success of clades. Evidence from the fossil record of macroevolutionary lags between the origin of a novelty and its ecological success demonstrates that novelty may be decoupled from innovation, and only definitions of novelty based on radicality (rather than generativity or consequentiality) can be assessed without reference to the subsequent history of the clade to which a novelty belongs. These considerations suggest a conceptual framework for novelty and innovation, involving: (i) generation of the potential for novelty; (ii) the formation of novel attributes; (iii) refinement of novelties through adaptation; (iv) exploitation of novelties by a clade, which may coincide with a new round of ecological or environmental potentiation; followed by (v) the establishment of innovations through ecological processes. This framework recognizes that there is little empirical support for either the dominance of ecological opportunity, nor abrupt discontinuities (often caricatured as ‘hopeful monsters’). This general framework may be extended to aspects of cultural and social innovation.     

Ecological opportunity and the origin of adaptive radiations

Ecological opportunity – through entry into a new environment, the origin of a key innovation or extinction of antagonists – is widely thought to link ecological population dynamics to evolutionary diversification. The population‐level processes arising from ecological opportunity are well documented under the concept of ecological release. However, there is little consensus as to how these processes promote phenotypic diversification, rapid speciation and adaptive radiation. We propose that ecological opportunity could promote adaptive radiation by generating specific changes to the selective regimes acting on natural populations, both by relaxing effective stabilizing selection and by creating conditions that ultimately generate diversifying selection. We assess theoretical and empirical evidence for these effects of ecological opportunity and review emerging phylogenetic approaches that attempt to detect the signature of ecological opportunity across geological time. Finally, we evaluate the evidence for the evolutionary effects of ecological opportunity in the diversification of Caribbean Anolis lizards. Some of the processes that could link ecological opportunity to adaptive radiation are well documented, but others remain unsupported. We suggest that more study is required to characterize the form of natural selection acting on natural populations and to better describe the relationship between ecological opportunity and speciation rates.     

Measuring the contribution of evolution to community trait structure in freshwater zooplankton

There are currently few predictions about when evolutionary processes are likely to play an important role in structuring community features. Determining predictors that indicate when evolution is expected to impact ecological processes in natural landscapes can help researchers identify eco-evolutionary ‘hotspots', where eco-evolutionary interactions are more likely to occur. Using data collected from a survey in freshwater cladoceran communities, landscape population genetic data and phenotypic trait data measured in a common garden, we applied a Bayesian linear model to assess whether the impact of local trait evolution in the keystone species Daphnia magna on cladoceran community trait values could be predicted by population genetic properties (within-population genetic diversity, genetic distance among populations), ecological properties (Simpson's diversity, phenotypic divergence) or environmental divergence. We found that the impact of local trait evolution varied among communities. Moreover, community diversity and phenotypic divergence were found to be better predictors of the contribution of evolution to community trait values than environmental features or genetic properties of the evolving species. Our results thus indicate the importance of ecological context for the impact of evolution on community features. Our study also demonstrates one way to detect signatures of eco-evolutionary interactions in communities inhabiting heterogeneous landscapes using survey data of contemporary ecological and evolutionary structure.     

Ecological and evolutionary responses in complex communities: implications for invasions and eco‐evolutionary feedbacks

It is easier to predict the ecological and evolutionary outcomes of interactions in less diverse communities. As species are added to communities, their direct and indirect interactions multiply, their niches may shift, and there may be increased ecological redundancy. Accompanying this complexity in ecological interactions, is also complexity in selection and subsequent evolution, which may feed back to affect the ecology of the system, as species with different traits may play different ecological roles. Drawing from my own work and that of many others, I first discuss what we currently understand about ecology and evolution in light of simple and diverse communities, and suggest the importance of escape from community complexity per se in the success of invaders. Then, I examine how community complexity may influence the nature and magnitude of eco‐evolutionary feedbacks, classifying eco‐evolutionary dynamics into three general types: those generating alternative stable states, cyclic dynamics, and those maintaining ecological stasis and stability. The latter may be important and yet very hard to detect. I suggest future directions, as well as discuss methodological approaches and their potential pitfalls, in assessing the importance and longevity of eco‐evolutionary feedbacks in complex communities. Synthesis The ecology, evolution and eco‐evolutionary dynamics of simple and diverse communities are reviewed. In more diverse communities, direct and indirect interactions multiply, species’ niches often shift, ecological redundancy can increase, and selection may be less directional. Community complexity may influence the magnitude and nature of eco‐evolutionary dynamics, which are classified into three types: those generating alternative stable states, cyclic dynamics, and those maintaining ecological stasis and stability. Strengths and pitfalls of approaches to investigating eco‐evolutionary feedbacks in complex field communities are discussed.