Editor’s Choice: Volume 110 Issue 3

The editor’s choice for our March issue is “The strength and direction of local (mal)adaptation depends on neighbor density and the environment” by Germain et al. Here, Associate Editor Chengjin Chu explains the importance of this research. 

Explicitly linking ecology and evolution to comprehensively reveal the interdependence structure of the entangled bank has been a long-standing issue due to the putative scale mismatch. Some advances have been achieved with the rapid development of phylogenetics and community genetics. However, the essential elements rooted in both subjects have failed to be satisfactorily merged into each other. On the one hand, biotic interactions especially from neighbouring organisms in natural communities have been less incorporated into the studies related to local adaptation. On the other hand, work on local adaptation usually focused on evolution under abiotic selection pressure without considering the impacts from neighbors. Germain et al. (2022) presented a fascinating example for how to merge them through competition models known well by ecologists and common gardens extensively used by evolutionary researchers.

Figure 1. Schematic of experimental design, including the systematic layout of transplanted individuals with (a) and without (b) neighbours, and the placement of focal individuals within interaction neighborhoods (c, d). Within each interaction neighbourhood, the abundance of every naturally-occurring species was recorded (the study mainly fit separate interaction coefficients αij for seven of the most abundant species).

This study was conducted at the McLaughlin Natural Reserve in Northern California, USA. Researchers performed two common garden transplant experiments (i.e. high-fitness garden vs. low-fitness garden) each using four populations (for each garden: one local, three foreign) of an invasive annual grass, Bromus hordeaceus, to explore the local adaptation of the species in the absence or presence of neighbours in natural communities (Fig. 1). The local (mal)adaptation was evaluated by the log fitness ratio of local/foreign populations. Then the per capita effects of neighbor species (species occurring with the radius of 7.5cm around the focal individual) on the fitness of B. hordeaceus were estimated by fitting multi-species competition models.

Figure 2. The effect of neighbours on the strength and direction of local adaptation (log fitness ratio of local/foreign populations) in the ‘high-fitness’ (a) and in ‘low-fitness’ (b) common gardens. The dashed grey lines are the boundary between local adaptation (local > foreign fitness) and local maladaptation (local < foreign fitness).

Two main findings inspired me emerged from this set of common garden experiments. First, adaptation or maladaptation of the species strongly depends on whether neighbors were removed and the environmental conditions (Fig. 2). Th presence of neighbors significantly increased the adaptation of the local population in the high-fitness garden, and the absence of neighbours led to extreme maladaptation in the low-fitness common garden. Secondly, the pairwise interaction coefficients (the effects of neighbors on B. hordeaceus) estimated from competition models depends on environmental conditions as well (Fig. 3). In the high-fitness garden, only two of seven species had distinguishable impacts on the fitness of B. hordeaceus. Some state-of-art method has been proposed recently to disentangle such key species interactions in diverse and heterogeneous communities, such as sparse modeling approach. In contrast, in the low-fitness garden, local B. hordeaceus populations suffered more competition than foreign populations from nearly every neighboring species.

Figure 3. Differences in the strength of per capita impacts of each neighbor species (seven of the most abundant species were evaluated here) on the conditional component of fitness of local vs. foreign B. hordeaceus individuals. (a, b) The per capita direct interaction coefficients of each neighbor species on the fitness of foreign (F) vs. local (L) B. hordeaceus populations. Negative values are competitive interactions and positive values for facilitative interactions.

In sum, local adaptation of B. hordeaceus was highly dependent on the surrounding biotic and abiotic environments. Put in other words, as Germain et al. (2022) stated, (1) testing local adaptation ignoring neighbours could result in erroneous estimates of its strength and direction in natural communities; and (2) the evolution of pairwise interactions is conditional on environment and unfolds differently among species. Future studies combining the reciprocal common garden experiments and population dynamics models are recommended for other species and communities, especially for perennial plants.

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