skip to main content

Title: Regional neutrality evolves through local adaptive niche evolution

Biodiversity in natural systems can be maintained either because niche differentiation among competitors facilitates stable coexistence or because equal fitness among neutral species allows for their long-term cooccurrence despite a slow drift toward extinction. Whereas the relative importance of these two ecological mechanisms has been well-studied in the absence of evolution, the role of local adaptive evolution in maintaining biological diversity through these processes is less clear. Here we study the contribution of local adaptive evolution to coexistence in a landscape of interconnected patches subject to disturbance. Under these conditions, early colonists to empty patches may adapt to local conditions sufficiently fast to prevent successful colonization by other preadapted species. Over the long term, the iteration of these local-scale priority effects results in niche convergence of species at the regional scale even though species tend to monopolize local patches. Thus, the dynamics evolve from stable coexistence through niche differentiation to neutral cooccurrence at the landscape level while still maintaining strong local niche segregation. Our results show that neutrality can emerge at the regional scale from local, niche-based adaptive evolution, potentially resolving why ecologists often observe neutral distribution patterns at the landscape level despite strong niche divergence among local communities.

more » « less
Award ID(s):
Author(s) / Creator(s):
; ; ; ;
Publisher / Repository:
Proceedings of the National Academy of Sciences
Date Published:
Journal Name:
Proceedings of the National Academy of Sciences
Page Range / eLocation ID:
p. 2612-2617
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Despite the well known scale‐dependency of ecological interactions, relatively little attention has been paid to understanding the dynamic interplay between various spatial scales. This is especially notable in metacommunity theory, where births and deaths dominate dynamics within patches (the local scale), and dispersal and environmental stochasticity dominate dynamics between patches (the regional scale). By considering the interplay of local and regional scales in metacommunities, the fundamental processes of community ecology—selection, drift, and dispersal—can be unified into a single theoretical framework. Here, we analyze three related spatial models that build on the classic two‐species Lotka–Volterra competition model. Two open‐system models focus on a single patch coupled to a larger fixed landscape by dispersal. The first is deterministic, while the second adds demographic stochasticity to allow ecological drift. Finally, the third model is a true metacommunity model with dispersal between a large number of local patches, which allows feedback between local and regional scales and captures the well studied metacommunity paradigms as special cases. Unlike previous simulation models, our metacommunity model allows the numerical calculation of equilibria and invasion criteria to precisely determine the outcome of competition at the regional scale. We show that both dispersal and stochasticity can lead to regional outcomes that are different than predicted by the classic Lotka–Volterra competition model. Regional exclusion can occur when the nonspatial model predicts coexistence or founder control, due to ecological drift or asymmetric stochastic switching between basins of attraction, respectively. Regional coexistence can result from local coexistence mechanisms or through competition‐colonization or successional‐niche trade‐offs. Larger dispersal rates are typically competitively advantageous, except in the case of local founder control, which can favor intermediate dispersal rates. Broadly, our models demonstrate the importance of feedback between local and regional scales in competitive metacommunities and provide a unifying framework for understanding how selection, drift, and dispersal jointly shape ecological communities.

    more » « less
  2. Premise

    The drivers of isolation between sympatric populations of long‐lived and highly dispersible conspecific plants are not well understood. In the Hawaiian Islands, the landscape‐dominant tree,Metrosideros polymorpha, displays extraordinary phenotypic differences among sympatric varieties despite high dispersibility of its pollen and seeds, thereby presenting a unique opportunity to investigate how disruptive selection alone can maintain incipient forms. StenophyllousM. polymorphavar.newelliiis a recently evolved tree endemic to the waterways of eastern Hawai'i Island that shows striking neutral genetic differentiation from its ancestor, wet‐forestM. polymorphavar.glaberrima, despite sympatry of these forms. We looked for evidence for, and drivers of, differential local adaptation of these varieties across the range ofM. polymorphavar.newellii.


    For paired populations of these varieties, we compared seedling performance under contrasting light conditions and a strong water current characteristic of the riparian zone. We also conducted a reciprocal transplant experiment and contrasted adult leaf anatomy.


    Results suggest that the riparian zone is harsh and that selection involving the mechanical stress of rushing water, and secondarily, light, led to significant reciprocal immigrant inviability in adjacent forest and riparian environments. The strongest adaptive divergence between varieties was seen in leaves and seedlings from the site with the sharpest ecotone, coincident with the strongest genetic isolation ofM. polymorphavar.newelliiobserved previously.


    These findings suggest that disruptive selection across a sharp ecotone contributes to the maintenance of an incipient riparian ecotype from within a continuous population of a long‐lived and highly dispersible tree species.

    more » « less
  3. Gralnick, Jeffrey A. (Ed.)
    ABSTRACT Microalgal cultures are often maintained in xenic conditions, i.e., with associated bacteria, and many studies indicate that these communities both are complex and have significant impacts on the physiology of the target photoautotroph. Here, we investigated the structure and stability of microbiomes associated with a diverse sampling of diatoms during long-term maintenance in serial batch culture. We found that, counter to our initial expectation, evenness diversity increased with time since cultivation, driven by a decrease in dominance by the most abundant taxa in each culture. We also found that the site from which and time at which a culture was initially collected had a stronger impact on microbiome structure than the diatom species; however, some bacterial taxa were commonly present in most cultures despite having widely geographically separated collection sites. Our results support the conclusion that stochastic initial conditions (i.e., the local microbial community at the collection site) are important for the long-term structure of these microbiomes, but deterministic forces such as negative frequency dependence and natural selection exerted by the diatom are also at work. IMPORTANCE Natural microbial communities are extremely complex, with many more species coexisting in the same place than there are different resources to support them. Understanding the forces that allow this high level of diversity has been a central focus of ecological and evolutionary theory for many decades. Here, we used stock cultures of diatoms, which were maintained for years in continuous growth alongside populations of bacteria, as proxies for natural communities. We show that the bacterial communities remained relatively stable for years, and there is evidence that ecological forces worked to stabilize coexistence instead of favoring competition and exclusion. We also show evidence that, despite some important regional differences in bacterial communities, there was a globally present core microbiome potentially selected for in these diatom cultures. Understanding interactions between bacteria and diatoms is important both for basic ecological science and for practical science, such as industrial biofuel production. 
    more » « less
  4. Abstract

    Effective management of threatened and exploited species requires an understanding of both the genetic connectivity among populations and local adaptation. The Olympia oyster (Ostrea lurida), patchily distributed from Baja California to the central coast of Canada, has a long history of population declines due to anthropogenic stressors. For such coastal marine species, population structure could follow a continuous isolation‐by‐distance model, contain regional blocks of genetic similarity separated by barriers to gene flow, or be consistent with a null model of no population structure. To distinguish between these hypotheses inO. lurida, 13,424 single nucleotide polymorphisms (SNPs) were used to characterize rangewide population structure, genetic connectivity, and adaptive divergence. Samples were collected across the species range on the west coast of North America, from southern California to Vancouver Island. A conservative approach for detecting putative loci under selection identified 235SNPs across 129GBSloci, which were functionally annotated and analyzed separately from the remaining neutral loci. While strong population structure was observed on a regional scale in both neutral and outlier markers, neutral markers had greater power to detect fine‐scale structure. Geographic regions of reduced gene flow aligned with known marine biogeographic barriers, such as Cape Mendocino, Monterey Bay, and the currents around Cape Flattery. The outlier loci identified as under putative selection included genes involved in developmental regulation, sensory information processing, energy metabolism, immune response, and muscle contraction. These loci are excellent candidates for future research and may provide targets for genetic monitoring programs. Beyond specific applications for restoration and management of the Olympia oyster, this study lends to the growing body of evidence for both population structure and adaptive differentiation across a range of marine species exhibiting the potential for panmixia. Computational notebooks are available to facilitate reproducibility and future open‐sourced research on the population structure ofO. lurida.

    more » « less
  5. Abstract

    Biological invasions are usually examined in the context of their impacts on native species. However, few studies have examined the dynamics between invaders when multiple exotic species successfully coexist in a novel environment. Yet, long‐term coexistence of now established exotic species has been observed in North American lady beetle communities. Exotic lady beetlesHarmonia axyridisandCoccinella septempunctatawere introduced for biological control in agricultural systems and have since become dominant species within these communities. In this study, we investigated coexistence via spatial and temporal niche partitioning amongH. axyridisandC. septempunctatausing a 31‐year data set from southwestern Michigan, USA. We found evidence of long‐term coexistence through a combination of small‐scale environmental, habitat, and seasonal mechanisms. Across years,H. axyridisandC. septempunctataexperienced patterns of cyclical dominance likely related to yearly variation in temperature and precipitation. Within years, populations ofC. septempunctatapeaked early in the growing season at 550 degree days, whileH. axyridispopulations grew in the season until 1250 degree days and continued to have high activity after this point.C. septempunctatawas generally most abundant in herbaceous crops, whereasH. axyridisdid not display strong habitat preferences. These findings suggest that within this regionH. axyridishas broader habitat and abiotic environmental preferences, whereasC. septempunctatathrives under more specific ecological conditions. These ecological differences have contributed to the continued coexistence of these two invaders. Understanding the mechanisms that allow for the coexistence of dominant exotic species contributes to native biodiversity conservation management of invaded ecosystems.

    more » « less