Predicting evolution in diverse communities

Following the outline of basic theory and evidence in chapters 7 and 8, this chapter sets the challenge of attempting to predict evolutionary dynamics in realistically diverse communities. Many challenges and opportunities facing human populations rely on being able to predict living systems. Even when a single focal species such as a pest or disease agent is of particular concern, its dynamics and responses to control measures always depend on interactions with a diverse set of other species. Even when the focus is on whole-ecosystem functioning, that depends on trait responses of constituent species. The chapter outlines several case studies where a multispecies evolutionary approach is required, including managing marine fisheries, controlling crop pests, and managing human microbiomes for improved health. To illustrate possible ways forwards, a model of evolution in a microbial community is presented, and possible methods for tracking evolution in diverse communities are discussed.

Species and speciation without sex

Species and speciation have been called phenomena of sexual organisms, and many of the concepts developed with sexuals in mind. It is clear theoretically, however, that asexuals should be affected in similar ways by the diversifying processes that cause speciation in sexuals. This chapter investigates evidence for species and speciation in organisms with alternative lifestyles. Bdelloid rotifers are presented as a putative case of asexual species, before the theory and evidence for species in bacteria is discussed. Both theoretically and empirically, the notion that bacteria do not diversify into species can be dismissed. There are interesting differences from eukaryotes, including lower rates of recombination and greater frequency of gene transfer between distant relatives, but neither of these seems to prevent divergence into independently evolving species, at least at core genome regions. Experimental evolution is a useful but neglected avenue to test these ideas further.

Introduction

This chapter explains what the book is about and highlights the range of processes and questions to be considered. The central thesis is that species represent more than a unit of taxonomy, they are a model of how diversity is structured and how groups of organisms evolve. All organisms live in diverse communities with hundreds of other species. Knowledge of what species are, how they form, and the genetic and ecological interactions among them is therefore vital both for understanding where diversity comes from and for predicting contemporary and future evolution. It is time for evolutionary biology to embrace the diversity of life.

Conclusions

This final chapter summarizes conclusions from the book and highlights a few general areas for future work. The species model for the structure of diversity is found to be useful and largely supported by current data, but is open to future tests against explicit alternative models. It is also a vital component for understanding and predicting contemporary evolution in the diverse systems that all organisms live in. The common evolutionary framework for microbial and multicellular life is highlighted, while drawing attention to current gaps in understanding for each type of organism. Future work needs to scale up to develop model systems of diverse assemblages and clades, including time-series data ranging from contemporary to geological scales. The imminent avalanche of genome data for thousands of individuals sampled within and between species is identified as a key challenge and opportunity. Finally, this chapter repeats the challenge that evolutionary biologists should embrace diversity and need to attempt to predict evolution in diverse systems, in order to deliver solutions of benefit to society.

The evidence for species—phenotypic and genetic clustering

This chapter discusses how to detect evolutionary species, and how to test whether species are real and to evaluate the alternative hypotheses for the structure of diversity described in chapter 2. After outlining evidence from phenotypic data, such as surveys of morphology, it describes population genetic methods for delimiting species from single-locus genetic data, of the kind gathered by DNA barcoding and taxonomy initiatives. All forms of life display the same pattern of discrete clustering of genetic variation that is indicative of the existence of independently evolving groups, that is, species. This is perhaps the best comprehensive evidence we have for the reality of species, but it leaves open many further questions about the causes of that pattern, and does not rule out more complex models for the structure of diversity.

How does species richness accumulate over time?

Species are units for understanding the evolution of diversity over large geographical scales and long timescales. This chapter investigates the processes causing proliferation and demise of species diversity within lineages and regions. Phylogenetic approaches have focused on documenting speciation and extinction rates, but mechanistic theory explaining variation in rates is scarce. Diversity patterns are better explained by geographical and ecological opportunity than by correlates of speciation and extinction rates per se. The neutral theory of biodiversity provides a framework that can be adapted to predict diversity patterns in terms of limits due to competition for space and resources, and species turnover (which cannot be detected directly from phylogenetic trees). These theories bring macroevolutionary and microevolutionary theories closer together. In particular, diversity patterns are the outcome of individual selection and dispersal playing out over long timescales. Some of the processes influencing species patterns can also structure diversity at higher taxonomic levels.

What are species?

This chapter looks at the ideas underpinning the definition of species. After outlining a standard model of species applicable to sexual organisms, it looks more broadly at the multiple forces that cause lineages to diversify into multiple distinct and independently evolving groups. ‘Independently evolving’ is defined and illustrated by reference to different kinds of organisms: sexuals, asexuals, prokaryotes, and hybridizing taxa. It then discusses whether forces of diversification truly act to generate discrete units, as proposed by the ‘species model’, and outlines some possible alternatives for the structure of diversity, such as a continuum of increasingly independent forms. The chapter emphasizes concrete theory that makes testable predictions to distinguish alternative models of the structure of diversity.

Species boundaries and contemporary evolution

Much of the evolutionary study of species is retrospective and reconstructs the past processes leading to extant diversity. Yet the nature of species and extent of diversity has profound implications for adaptation to ongoing environmental and biotic change. This chapter considers the significance of species and species boundaries for contemporary evolution. Simple theory and evidence is presented, showing how partial gene flow between co-occurring species alters the dynamics of evolution in changing environments. The chapter then focuses on gene transfer in microbial populations, showing how plasmids and phage target transfer to particular subsets of genes, and thereby optimize adaptation in fluctuating environments. The costs and benefits depend on the ecological interactions among the donor and recipient species. Different mechanisms have a different range of transfer, with phage being mainly restricted to species, but plasmids often transferring traits across greater taxonomic distances.

What causes speciation?

The balance of evidence from earlier chapters is largely consistent with the reality of species units. This chapter therefore moves on to investigate what causes new species to form. This process involves a series of steps involving the origin of new diversifying conditions, the genetic response of the organisms to those conditions, the persistence of the newly diverged species, and the re-establishment of diversifying conditions in one or more of the descendants to restart the process. Distinguishing the role of geographical isolation and divergent selection in this process, the chapter reviews the theory and evidence for the causes of speciation from systematic evidence across whole clades. In particular, it focuses on whether speciation depends more on the extrinsic conditions favouring divergence or the intrinsic responses of the affected organisms. More integrated theory and coordinated efforts to uncover speciation dynamics for whole clades or regions are needed to answer these questions.

Why are there species?

This chapter continues the discussion of evolutionary methods of species delimitation by exploring how multilocus methods can be used to delimit reproductively isolated groups, and how genetic and trait data can be used in concert to delimit groups that experience divergent selection. These methods provide a way to evaluate the different mechanisms leading to cohesion within species and divergence between them. Multilocus data are scarcer at present than single-locus data discussed in chapter 3, and more work is needed to test alternative hypotheses for the pattern of reproductive isolation—does it generally fall into discrete units or are there broader or gradually declining rates of gene exchange? Divergent selection is less commonly used as a metric for delimiting species, and possible new methods are introduced. Possible uses of whole-genome data are discussed for combining these approaches and testing whether reproductive isolation and divergent selection tend to overlap to generate species or whether more complex models of diversity are required.