Brain Size in Hylarana Guentheri Seems Unaffected by Variation in Temperature and Growth Season
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Animal Biology 67 (2017) 209–225 brill.com/ab Brain size in Hylarana guentheri seems unaffected by variation in temperature and growth season Jun Gu1, Da Yong Li1, Yi Luo1, Song Bei Ying1, Lan Ya Zhang1, Qing Mao Shi2, Jian Chen2, Shi Peng Zhang2, Zhao Min Zhou1,∗ and Wen Bo Liao1,∗ 1 Key Laboratory of Southwest China Wildlife Resources Conservation (Ministry of Education), China West Normal University, Nanchong 637009, Sichuan, China 2 Micangshan Nature Reserve, Wangcang, 628200, Sichuan, China Submitted: June 3, 2017. Final revision received: August 21, 2017. Accepted: August 31, 2017 Abstract Brain size varies dramatically between vertebrate species. Two prominent adaptive hypotheses – the Cognitive Buffer Hypothesis (CBH) and the Expensive Brain Hypothesis (EBH) – have been proposed to explain brain size evolution. The CBH assumes that brain size should increase with seasonality, as the cognitive benefits of a larger brain should help overcoming periods of food scarcity via, for exam- ple, increased behavioral flexibility. Alternatively, the EBH states that brain size should decrease with seasonality because a smaller brain confers energetic benefits in periods of food scarcity. Here, to test the two adaptive hypotheses by studying the effects of variation in temperature and growth season on variations in overall brain size and the size of specific brain regions (viz. olfactory nerves, olfactory bulbs, telencephalon, optic tectum and cerebellum) among Hylarana guentheri populations. Inconsis- tent with the predictions of both the EBH and the CBH, variation in temperature and growth season did not exhibit correlations with overall brain size and the size of brain regions across populations. Hence, our data do not provide support for either the EBH or the CBH to explain brain size variation in H. guentheri. Furthermore, brain size variation did not differ between males and females in this species. Our findings suggest that both the variation in temperature and growth season did not shape the variation in brain size in H. guentheri. Keywords Brain; brain size evolution; cognitive buffer hypothesis; expensive brain hypothesis; flexibility; frog; habitats; Hylarana guentheri; plasticity; seasonality; temperature ∗ ) Corresponding authors; e-mails: [email protected]; [email protected] © Koninklijke Brill NV, Leiden, 2017 DOI 10.1163/15707563-00002533 Downloaded from Brill.com09/23/2021 07:29:58PM via free access 210 J. Gu et al. / Animal Biology 67 (2017) 209–225 Introduction Brain size varies dramatically between vertebrate species (Striedter, 2005; Zeng et al., 2016). Several adaptive hypotheses have been proposed to explain the evolution of brain size in vertebrates. Most of these hypotheses assume that due to its cog- nitive benefits a larger brain is positively selected (e.g. Tomasello, 1999; Deaner et al., 2007; Reader et al., 2011; Vincze, 2016). For example, the Cognitive Buffer Hy- pothesis (CBH; see Allmann et al., 1993; Sol, 2009) states that a relatively larger brain allows for increased behavioral flexibility, which facilitates the behavioral buffering of unpredictable changes in environments (Lefebvre et al., 1997; Sayol et al., 2016). Central to the CBH is that larger-brained species should perform better in more seasonal habitats where cognitive demands are stronger because it is dif- ficult to locate the available food sources in space or time (Sol et al., 2005, 2008). A recent study across 1200 bird species found support for the CBH in a seasonal- ity context, as brain size and environmental variation showed a positive association (Sayol et al., 2017). Environmental harshness, reflected by minimum winter tem- peratures positively correlates with brain size in birds (Vincze, 2016). However, because the brain is among the most energetically costly organs in the vertebrate body (Mink et al., 1981), evolution of an enlarged brain requires either a decrease in other energetic requirements, or an increase in overall energy consump- tion (Fonseca-Azevedo & Herculano-Houzel, 2012). This energetic perspective on brain size evolution is generally termed the Expensive Brain Hypothesis (EBH, Aiello & Wheeler, 1995). Central to the EBH is that animals experiencing periodic energy shortages, which are typical for instable environments, may reduce their brain size so they can save energy to endure those periods. Brain size may therefore be negatively related with experienced seasonality, especially in terms of the dura- tion of periods of low food availability (Isler & van Schaik, 2009). The strongest evidence in favor of the EBH stems from strepsirrhine primates where seasonality is negatively correlated with relative brain size (van Woerden et al., 2010). In the same group of animals, however, the CBH also found support (van Woerden et al., 2011). The CBH and the EBH predict relationships between a species’ overall brain size and the seasonality of its habitat; for brain regions such a hypothesis does not exist. The mosaic brain evolution model emphasize that relative total brain size is larger in resident species, especially those living in harsher climates (Vincze, 2016), but this does not imply a uniform change in all brain regions (see Vincze et al., 2015). A rich literature on neuro-ecology shows that variations in brain regions are correlated with habitat structures, diet quality and predation pressure across species in a number of taxa (Clutton-Brock & Harvey, 1980; Huber et al., 1997; Safi & Dechmann, 2005; Dunbar & Shultz, 2007; Pollen et al., 2007; Yopak et al., 2010; West, 2014; Wu et al., 2016). For example, the relative sizes of forebrain and telencephalon show positive correlations with habitat complexity in fishes (Hu- ber et al., 1997; Pollen et al., 2007). Furthermore, piscivorous species have larger Downloaded from Brill.com09/23/2021 07:29:58PM via free access J. Gu et al. / Animal Biology 67 (2017) 209–225 211 relative sizes of olfactory bulbs and optic tecta than insectivorous and zooplank- tivorous species (Huber et al., 1997). Meanwhile, environmental pressure selects for marked variations in the sizes of brain regions in the same species (Chrispo & Chapman, 2010; Kotrschal et al., 2017). For example, the black-capped chickadees experiencing harsh northern climates have a larger hippocampal size than those living in mild southern climates (Chrispo & Chapman, 2010). Predation pressure can also have an effect, and selects for larger forebrain and optic tectum size in guppies (Poecilia reticulata; Kotrschal et al., 2017). Moreover, populations expe- riencing long growth seasons are characterized by having relatively large olfactory bulbs and optic tecta in the Andrew’s toad (Bufo andrewsi; Jiang et al., 2015). However, the relative size of none of the brain regions of the Asian grass frog (Fe- jervarya limnocharis) is correlated with variation in temperature and growth season related to environmental habitats (Mai et al., 2017). Hence, the effects of variation in temperature and growth season on the evolution of the overall brain and spe- cific brain regions at the intraspecific level needs to be explored in more species of frogs. Environmental seasonality – expressed in increased variability in mean tempera- ture and growth season (if applicable) – often determines food availability in frogs, mostly via influencing the abundance of insects (Zhang & Zhang, 2010; Shi et al., 2011). Because insect mortality is often determined by the degree of environmen- tal seasonality across species (Morecroft et al., 2002; Savage et al., 2004; Dang & Chen, 2011; Chen et al., 2016b), more variation in temperature and shorter growth season therefore results in less food availability. In the present study, we investi- gated the patterns and possible causes of variation in brain size and the sizes of specific brain regions (viz. olfactory nerves, olfactory bulbs, telencephalon, optic tectum and cerebellum) across six Hylarana guentheri populations. In particular, we examine the predictions of the CBH and EBH by investigating the relationships between relative size of the overall brain and brain regions with environmental sea- sonality. Materials and methods Study species The Günther’s frog (Hylarana guentheri) is widely distributed in the subtropical forests in China at elevations ranging from 500 to 1100 m (Fei & Ye, 2001). The species experiences a changing activity period. Males actively search for females and attract them by advertisement calls. In this species, mating and egg-laying ex- tends from March to May, as a prolonged breeder (Wells, 1977). There is a positive relationship between age and body size within each sex (Li et al., 2010). Study site All adult frogs were collected from six populations during the breeding seasons along a 420-km latitudinal and 341-m altitudinal transect across the Hunan, Hubei Downloaded from Brill.com09/23/2021 07:29:58PM via free access 212 J. Gu et al. / Animal Biology 67 (2017) 209–225 Figure 1. Topographic maps showing the locations of the six populations of Hylarana guentheri in China. and Sichuan provinces in China (fig. 1). The three study sites located in Hunan have an annual average temperature of 15.2-18.7°C and an annual total precipitation of 958-1185 m. The site from Hubei has an annual average temperature of 17-18.3°C and annual total precipitation of 897-1350 mm. The two sites from Sichuan have an annual average temperature of 18.3-20.3°C and annual total precipitation of 845- 889 mm. We captured all individuals from the six populations in paddy fields, pools and neighboring