UC Berkeley UC Berkeley Previously Published Works Title Island time and the interplay between ecology and evolution in species diversification. Permalink https://escholarship.org/uc/item/2tk8b8rq Journal Evolutionary applications, 9(1) ISSN 1752-4571 Author Gillespie, Rosemary G Publication Date 2016 DOI 10.1111/eva.12302 Peer reviewed eScholarship.org Powered by the California Digital Library University of California Evolutionary Applications Evolutionary Applications ISSN 1752-4571 REVIEW AND SYNTHESES Island time and the interplay between ecology and evolution in species diversification Rosemary G. Gillespie Department of Environmental Science, Policy, and Management, University of California, Berkeley, CA, USA Keywords Abstract adaptive radiation, biodiversity, chronosequence, ecomorph, Hawaiian Islands, Research on the dynamics of biodiversity has progressed tremendously over Pacific, spiders. recent years, although in two separate directions – ecological, to determine change over space at a given time, and evolutionary, to understand change over Correspondence time. Integration of these approaches has remained elusive. Archipelagoes with a Rosemary G. Gillespie, Department of known geological chronology provide an opportunity to study ecological interac- Environmental Science, Policy, and tions over evolutionary time. Here, I focus on the Hawaiian archipelago and Management, University of California, Berkeley, CA 94720-3114, USA. summarize the development of ecological and evolutionary research; I emphasize Tel.: +1-510-6423445; spiders because they have attributes allowing analysis of ecological affinities in e-mail: [email protected] concert with diversification. Within this framework, I highlight recent insights from the island chronosequence, in particular the importance of (i) selection and Received: 16 March 2015 genetic drift in generating diversity; (ii) fusion and fission in fostering diversifica- Accepted: 30 July 2015 tion; and (iii) variability upon which selection can act. Insights into biodiversity dynamics at the nexus of ecology and evolution are now achievable by integrating doi:10.1111/eva.12302 new tools, in particular (i) ecological metrics (interaction networks, maximum entropy inference) across the chronosequence to uncover community dynamics and (ii) genomic tools to understand contemporaneous microevolutionary change. The work can inform applications of invasion and restoration ecology by elucidating the importance of changes in abundances, interaction strengths, and rates of evolutionary response in shaping biodiversity. our understanding of how regional large-scale processes Introduction contribute to diversity at the local scale. A second approach A grand challenge in understanding the origins of biodiver- uses detailed phylogenetic hypotheses across entire lineages sity is to ‘disentangle the influence of evolutionary and his- to provide insights into change over evolutionary time. torical processes operating at larger spatiotemporal scales With the increasing availability of data across the diversity from ecological processes operating at smaller scales’ (Les- of life and broad spatial scales, this second framework can sard et al. 2012). What makes this difficult is that ecological be coupled with data on current ecological traits and pat- and evolutionary processes form a continuum and, while terns of richness (Wiens et al. 2011; Anacker and Harrison we can observe and test local ecological phenomena, we 2012) to provide tests of how the interplay between ecolog- must usually infer evolutionary processes from current ical and evolutionary processes has shaped present-day bio- observations, often at larger spatial and temporal scales. diversity (Graham et al. 2014). A missing element in both Efforts to reconcile the interaction of ecological and evolu- approaches is an understanding of how short-term ecologi- tionary processes have largely adopted one of two cal processes, such as colonization and ecological fitting, approaches. The first makes maximal use of extensive sets can together give rise to larger and longer term processes of of spatial data for broad comparative studies (Chase and adaptation and diversification. In particular, understanding Myers 2011; Belmaker and Jetz 2012); these studies use how community-level ‘ecological’ processes play out into sophisticated approaches, with clustering analysis, network longer term ‘evolutionary’ processes is a black box in the modularity analysis, and assemblage dispersion fields to understanding of biodiversity dynamics. Thus, a funda- define regional species pools (Carstensen et al. 2013). The mental goal in biodiversity research is to add a dynamic far-reaching scope of these studies has added immensely to framework to community ecology, which tends to view © 2015 The Author. Evolutionary Applications published by John Wiley & Sons Ltd. This is an open access article under the terms of the Creative 53 Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. Integration of ecology and evolution on islands Gillespie species as a fairly static pool (Mittelbach and Schemske 2010). Lacking to date is progress advancing these theories 2015); this approach would allow a much needed under- from the static to the dynamic so as to understand how standing of the ecological/evolutionary interplay involved variables change during community assembly, including in the formation of biodiversity. effects of invasion and extinction. Ecological insights into processes shaping species diversity Difficulty of extrapolating ecological insights over evolutionary time Until recently, ecological approaches to understanding parameters that dictate species composition, diversity, and Adaptation and diversification are frequently studied inde- community stability at a site primarily used one of two pendently from analyses of community assembly and contrasting approaches. First, growing out of classic deter- structure, although there is increasing interest in linking ministic community ecology theory, manipulations of the two, for example, in models of climate envelopes model vignette communities (with manageable species sub- (Sutherst et al. 2007) and food webs (Loeuille and Loreau sets in simplified mesocosms) or laboratory systems, cou- 2005; Johnson and Stinchcombe 2007). Attempts to assess pled with simple dynamic theory, allowed tests for the role of ecological processes in population differentia- alternative mechanisms of local community interactions, tion and speciation have been limited due to the difficulty such as predation or competition as limits to local diversity of making observations over evolutionary time, coupled (e.g. Huffaker 1958; Paine 1966; Wilbur 1997; May 2001; with the complexity of most natural systems. However, Steiner et al. 2006). The main limitation of this approach is much progress has been made through detailed studies of whether the results are relevant to more complex natural recent divergence (Schluter 2003, 2009) and associated systems. In contrast, comparative approaches have applied micro-evolutionary change (e.g. Roesti et al. 2014), statistical analysis of species composition of whole commu- although even in these studies, it is difficult to assess how nities along abiotic gradients or time series to infer pro- short-term effects of ecological interactions may translate cesses responsible for patterns of diversity (e.g. Pianka into species formation (Losos 2010). Rapidly diversifying 1966; Rohde 1992). The main limitation here is that many bacterial communities have provided microcosm systems hypotheses might explain similar patterns, making infer- allowing insights into the dynamics of diversification ences on causation difficult (Palmer 1994). (Fukami et al. 2007; Meyer and Kassen 2007), but the From a theoretical perspective, exciting progress in challenge is to apply this knowledge more broadly (Gille- understanding community structure comes from mecha- spie and Emerson 2007). Each of these research angles, nistic models that can successfully predict strong central while highlighting the importance of integrating the fields tendencies in quantitative food web patterns (Dunne 2006; of community ecology and evolutionary biology to under- Williams and Martinez 2008) and the effects of species loss stand processes involved in generating and maintaining and other dynamic population and community-level prop- biodiversity (Seehausen 2009; Palkovacs and Hendry erties (Berlow et al. 2009; Romanuk et al. 2009). The devel- 2010), also emphasizes the need for a well-defined and opment of unified theories (neutral, continuum, simple system in order to measure and identify interac- metapopulation, fractal, clustered Poisson, MaxEnt) that tions (biotic and abiotic) and feedbacks. establish a common set of rules to explain processes previ- To sum up, species diversity unfolds over evolutionary ously thought to be distinct has added richly to the under- time in a highly complex manner that involves the entire standing of biodiversity (Hubbell 2001; McGill 2010). One community of organisms; the challenge is to find a study particularly powerful (but currently entirely spatial) theory, system that is simple enough to get a handle on all of the derived from maximum information entropy is the maxi- complexity, the history, the geography, and evolutionary mum entropy theory of ecology (METE; Harte 2011; Harte adaptation. Islands – in particular remote oceanic islands and Newman