Basal Resistance Enhances Warming Tolerance of Alien Over Indigenous Species Across Latitude
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Basal resistance enhances warming tolerance of alien over indigenous species across latitude Charlene Janion-Scheepersa,1, Laura Phillipsa, Carla M. Sgròa, Grant A. Duffya, Rebecca Hallasa, and Steven L. Chowna aSchool of Biological Sciences, Monash University, Melbourne, VIC 3800, Australia Edited by David L. Denlinger, Ohio State University, Columbus, OH, and approved November 21, 2017 (received for review September 4, 2017) Soil systems are being increasingly exposed to the interactive effects meta-analyses (19)], the F2 generation of populations of each spe- of biological invasions and climate change, with rising temperatures cies to overcome parental effects and the potential for laboratory expected to benefit alien over indigenous species. We assessed this adaptation (20), and taking account of the influence of phylogenetic expectation for an important soil-dwelling group, the springtails, by relatedness (21), we investigated both basal thermal tolerance and determining whether alien species show broader thermal tolerance the extent of phenotypic plasticity in the upper critical thermal limits. limits and greater tolerance to climate warming than their indigenous Although phenotypic plasticity of thermal tolerance traits may counterparts. We found that, from the tropics to the sub-Antarctic, only play a limited role in reducing exposure to climate change in alien species have the broadest thermal tolerances and greatest some ectotherms (22), it has been identified as a potentially signif- tolerance to environmental warming. Both groups of species show icant mediator of responses to thermal challenge (23), including in little phenotypic plasticity or potential for evolutionary change in springtails (9, 24). Phenotypic plasticity is also thought to be a major tolerance to high temperature. These trait differences between alien contributor to the success of invasive species (25, 26). In addition, total thermal tolerance range and lower critical thermal limits play a and indigenous species suggest that biological invasions will exacer- role in determining range shifts in response to environmental change bate the impacts of climate change on soil systems, with profound (16). Thus, we not only assessed basal tolerance, but also phenotypic implications for terrestrial ecosystem functioning. plasticity for both upper and lower critical thermal limits. We eval- uated whether climate-related variation in upper and lower critical climate change | introduced species | soil fauna | thermal limits | thermal limits, thermal tolerance range, and warming tolerance— laboratory evolution the difference between species’ upper critical thermal limits and SCIENCES maximum environmental temperatures (17)—differ systematically ENVIRONMENTAL he impacts of climate change and biological invasions con- between the indigenous and alien springtail species. Tests were Ttinue to increase in magnitude (1, 2), yet investigation of their conducted using phylogenetic generalized least squares (PGLS) interactions remains fragmented and incomplete (3). The general (21), and a phylogenetic tree constructed from molecular markers expectation is that such interactions will benefit alien over in- to take into account phylogenetic signal in the traits measured. digenous species, and thus have negative consequences for native Evolutionary responses have the potential to reduce substantially biodiversity (4). Soil systems are globally important reservoirs of the impacts of climate change on populations (27, 28). Therefore, diversity, influence aboveground ecological dynamics, and are criti- we also examined the extent to which thermal traits might evolve in cal for food security (5). They are also highly susceptible to climate springtails and whether this potential differs between indigenous change and to biological invasions, which both have major effects on and alien species. We used laboratory natural selection (29) to as- soil ecosystem functioning and are expected to interact to the det- sess the extent of evolutionary potential in the critical thermal limits riment of these systems (6, 7). Understanding how climate change– invasion interactions will play out in soil systems is, therefore, Significance pressing (8). For the soil biota, increasing temperature is one of the most significant components of climate change (9). Differential fit- How climate change and biological invasions interact to affect ness effects of rising temperatures on indigenous compared with biodiversity is of major concern to conservation. Quantitative evi- alien species must necessarily be mediated by consistent thermal dence for the nature of climate change–invasion interactions is, trait differences between these two groups of species (10). More- however, limited. For the soil ecosystem fauna, such evidence is over, if such effects are general, these trait differences between alien nonexistent. Yet across the globe, soil-dwelling animals regulate and indigenous species should be maintained across a broad lat- belowground functioning and have pronounced influences on itudinal—and hence climatic—range. No study has yet evaluated for aboveground dynamics. Using springtails as an exemplar taxon, any group of soil macrobiota whether such latitudinally extensive widely known to have species-specific effects on below- and differences in thermal traits exist that advantage alien species under aboveground dynamics, we show that across a wide latitudinal warming conditions, and thus whether forecast impacts are likely to span (16–54°S), alien species have greater ability to tolerate climate be realized. change-associated warming than do their indigenous counterparts. To assess this expectation, we investigated the thermal limits to The consequences of such consistent differences are profound activity in 16 alien and 14 indigenous species of springtails (Col- given globally significant invasions of soil systems by springtails. lembola) spanning a climatic gradient from the Australian tropics (16°S) to south of the Antarctic Polar Front (54°S) (Fig. 1). Author contributions: C.J.-S., L.P., C.M.S., and S.L.C. designed research; C.J.-S., L.P., C.M.S., Springtails are a globally distributed, functionally significant com- R.H., and S.L.C. performed research; C.J.-S., L.P., G.A.D., and S.L.C. analyzed data; and ponent of the soil biota (5, 11). The group includes many alien C.J.-S., L.P., C.M.S., G.A.D., R.H., and S.L.C. wrote the paper. species that have invaded soil systems from the polar regions to the The authors declare no conflict of interest. tropics (6, 12). Critical thermal limits to activity form a useful proxy This article is a PNAS Direct Submission. for adult fitness because organisms are incapable of movement This open access article is distributed under Creative Commons Attribution-NonCommercial- outside of these limits, thus reducing fitness (13, 14), with de- NoDerivatives License 4.0 (CC BY-NC-ND). mographic effects reflected in associations between critical thermal Data deposition: The data used for this work are deposited in Monash Figshare limits and geographic ranges in several taxa (15, 16). Upper critical (10.4225/03/59fa71b5291c8). thermal limits are also now widely used to assess tolerance to cli- 1To whom correspondence should be addressed. Email: charlene.janionscheepers@ mate change-associated warming in a wide range of organisms (17, monash.edu. 18). Using a single consistent method [in contrast with multiple This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. methods represented in and which complicate interpretations of 1073/pnas.1715598115/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1715598115 PNAS Early Edition | 1of6 Downloaded by guest on September 25, 2021 Fig. 1. Geographic variation in basal critical thermal limits and their phenotypic plasticity across Australia. Violin plots display the frequency density of indi- vidual critical thermal limits data (smoothed with a Gaussian kernel) for control and acclimation pop- ulations of each species. In each case the control value is the basal tolerance of the species, whereas the other values refer to experimental acclimations (low, medium, high; 5 °C below, 5 °C above, 10 °C above control values, respectively) (SI Appendix,Ta- ble S8). Soil temperature contours represent the median daytime temperature 2.5-cm below the soil surface, estimated using methods detailed in SI Ap- pendix. Lord Howe Island (A: 31.5°S, 159.0°E) and the sub-Antarctic sites of South Georgia (B: 54.2°S, 36.6°W, south of the Antarctic Polar Front) and Macquarie Island (C: 54.5°S, 158.9°E) are not shown. Indigenous and alien species are indicated by green circles and orange circles, respectively, adjacent to species names. of an indigenous and alien species from the tropics and another difference in tolerance range, of on average 3.4 ± 1.1 °C (Fig. 2C), such pair of species from the temperate zone, held at elevated was found between the indigenous and alien species, with strong temperatures just below those that substantially depress fitness in phylogenetic signal in the trait (Table 1). Thus, overall, upper and these species, so reflecting extreme environmental conditions. lower critical temperatures varied in similar ways with microhabitat temperature across latitude, resulting in no microhabitat-associated Results variationinthermaltolerancerange. Consistently large differences Critical Limits and Warming Tolerance. Although critical thermal among the indigenous and alien species were, however,