Local Adaptation in Thermal Tolerance for a Tropical Butterfly Across Ecotone and Rainforest Habitats

UCLA UCLA Previously Published Works Title Local adaptation in thermal tolerance for a tropical butterfly across ecotone and rainforest habitats. Permalink https://escholarship.org/uc/item/85w6t4qv Journal Biology open, 10(4) ISSN 2046-6390 Authors Dongmo, Michel AK Hanna, Rachid Smith, Thomas B et al. Publication Date 2021-04-06 DOI 10.1242/bio.058619 Peer reviewed eScholarship.org Powered by the California Digital Library University of California © 2021. Published by The Company of Biologists Ltd | Biology Open (2021) 10, bio058619. doi:10.1242/bio.058619 RESEARCH ARTICLE Local adaptation in thermal tolerance for a tropical butterfly across ecotone and rainforest habitats Michel A. K. Dongmo1,2,3, Rachid Hanna1, Thomas B. Smith4, K. K. M. Fiaboe1, Abraham Fomena2 and Timothy C. Bonebrake3,* ABSTRACT composition, and changes in phenology (Scheffers et al., 2014). Thermal adaptation to habitat variability can determine species Physiologically based models show that tropical ectotherms may be vulnerability to environmental change. For example, physiological more vulnerable to climate warming than temperate species by tolerance to naturally low thermal variation in tropical forests species virtue of being adapted to lower thermal variation (Deutsch et al., may alter their vulnerability to climate change impacts, compared with 2008). However, the sensitivity of ectotherms to warming is also open habitat species. However, the extent to which habitat-specific structured by experienced thermal variation across elevation and differences in tolerance derive from within-generation versus across- habitat (Sunday et al., 2014; García-Robledo et al., 2016). For generation ecological or evolutionary processes are not well species with broad distributions, populations may occur in diverse characterized. Here we studied thermal tolerance limits of a Central habitat types where selective pressures (e.g. temperature) during African butterfly (Bicyclus dorothea) across two habitats in Cameroon: a ontogeny may act differentially and have significant repercussions thermally stable tropical forest and the more variable ecotone between on physiological traits (Hoffmann et al., 2003). Local adaptation to rainforest and savanna. Second generation individuals originating from thermal conditions can thus lead to population-specific responses the ecotone, reared under conditions common to both populations, (Somero, 2010; Kaspari et al., 2015; Nadeau et al., 2017). exhibited higher upper thermal limits (CTmax) than individuals Recent studies in tropical ecosystems have found that forest species of originating from forest (∼3°C greater). Lower thermal limits (CTmin) ectotherms tend to have lower tolerance to warming because they are were also slightly lower for the ecotone populations (∼1°C). Our results restricted to more stable thermal regimes and might be especially are suggestive of local adaptation driving habitat-specific differences in vulnerable to climate change compared with more open habitat species thermal tolerance (especially CTmax) that hold across generations. (Huey et al., 2009; Frishkoff et al., 2015; Bonebrake et al., 2016; Such habitat-specific thermal limits may be widespread for tropical Nowakowski et al., 2017). However, ectotherms do have the ability to ectotherms and could affect species vulnerability to environmental behaviorally avoid extreme temperatures through thermoregulatory change. However, microclimate and within-generation developmental activities and experiencing diverse microclimates at multiple spatial processes (e.g. plasticity) will mediate these differences, and scales (Sunday et al., 2014; Bonebrake et al., 2014; Pincebourde and determining the fitness consequences of thermal variation for Woods, 2020). Furthermore, thermal tolerance differences in populations ecotone and rainforest species will require continued study of both across habitats can sometimes be diminished by developmental within-generation and across-generation eco-evolutionary processes. conditions; Montejo-Kovacevich et al. (2020), for example, found that for tropical Heliconius erato butterflies, differences in heat tolerance This article has an associated First Person interview with the first across elevation were nearly erased after rearing in a common garden. author of the paper. Measured thermal traits are ultimately a combination of natural selection/genetics, intergenerational plasticity (offspring traits KEY WORDS: Climate change, Common garden, Ecotone, Thermal affected by parental environmental conditions), developmental tolerance, Bicyclus dorothea plasticity, and acclimation or reversible plasticity (Llewelyn et al., 2018). Indeed, acclimation within generations can drive CTmax INTRODUCTION variation for amphibians across habitats (Kristensen et al., 2008; It is presently widely accepted that ongoing climate warming has Gunderson and Stillman, 2015; Simon et al., 2015). Upper thermal clear and widespread consequences for biodiversity including local limits for terrestrial ectotherms appear to be fairly constrained – but extinction, population declines, shifts in community structure and details for how such limits vary with acclimation and plasticity across habitats or microhabitats are needed (Hoffmann et al., 2013). 1International Institute of Tropical Agriculture (IITA), PO Box 2008 (Messa), Specifically, knowing the extent to which differences in habitat- Yaoundé-Cameroon, Yaoundé, Cameroon. 2Laboratory of Parasitology and specific thermal tolerance can be explained by processes within or Ecology, Faculty of Science, University of YaoundéI PO Box 812, Yaoundé- Cameroon. 3Division of Ecology & Biodiversity, School of Biological Sciences, The across generations can help elucidate vulnerability to climate University of Hong Kong, Hong Kong SAR, China. 4Department of Ecology and change, especially for tropical ectotherms. Evolutionary Biology and Institute of Environment and Sustainability, University of Though tropical Africa is dominated by rainforest, there is California, Los Angeles (UCLA), Los Angeles, CA 90095, USA. important variation in ecosystem physiognomy; ecotones that *Author for correspondence ([email protected]) consist of a mosaic of woody or herbaceous savanna and gallery forests representing a key habitat in the landscape and region thought M.A.K.D., 0000-0002-0509-5227; T.C.B., 0000-0001-9999-2254 to be important for speciation (Smith et al., 1997). Rainforest climates This is an Open Access article distributed under the terms of the Creative Commons Attribution tend to be constant and regular due to high tree density and high License (https://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed. annual average precipitation. Ecotones in contrast have relatively variable climates and consist of a mosaic of homogenous vegetation Received 3 February 2021; Accepted 4 March 2021 types leading to more open canopy spaces than rainforests. In this Biology Open 1 RESEARCH ARTICLE Biology Open (2021) 10, bio058619. doi:10.1242/bio.058619 study we investigated the role of habitat in structuring thermal limits, individuals reared in a common environment, indicates a level of critical thermal maximum (CTmax) and minimum (CTmin), for habitat-specific adaptation in thermal tolerance for this species. We Bicyclus dorothea (Cramer, 1779), a nymphalid butterfly found in also found that CTmin was lower for ecotone populations, but to a both forest and ecotone habitats in many tropical African countries smaller extent (by ∼1°C). At least for large spatial gradients then (Dongmo et al., 2017). Bicyclus dorothea exhibits differential (hundreds of kilometers, Fig. 1), our results show that local variability in wing morphology across ecotone and forest habitats adaptation to habitat climatic conditions may result in differential ecotone in Cameroon (Dongmo et al., 2018). We hypothesized that thermal tolerances for species which may have consequences for B. dorothea populations from the ecotone would have wider thermal vulnerability to environmental and climatic change. tolerance breadths than forest populations (reflecting the greater Our results support the evidence of local adaptation playing a role thermal variation in those environments) that would be preserved in variable thermal tolerance limits across habitat, as has been after lab-rearing under common conditions. shown in a variety of systems including tropical beetles by García- Robledo et al. (2016) and tropical lizards by Moritz et al. (2012). RESULTS However, variation in thermal limits can also be a consequence of We collected CTmin and CTmax data for a total of 399 s generation developmental effects, ontogenetic changes, and phenotypic butterflies originating across all sites. The mean CTmin (±s.e.) for plasticity (Bowler and Terblanche, 2008; Kellermann and Sgrò, ecotone females (4.5±0.15, n=110) and males (4.4±0.14, n=106) 2018). As an example, and in contrast with our own findings, was lower than forest females (5.1±0.16, n=89) and males (4.9± Montejo-Kovacevich et al. (2020) found little difference in thermal 0.15, n=94); habitat affected CTmin (P<0.001) while sex and site did tolerance (knockdown time) for a tropical butterfly species across not (P>0.50; Fig. 2, Table 1). The mean CTmax (±s.e.) for ecotone elevation following rearing in a common garden environment, females (45.9±0.14, n=110) and males (46.1±0.15, n=106) was despite finding significant differences

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