We explored the relationship between elevational climatic zonation and speciation by comparing latitudinal patterns of variation in the thermal regimes of 93 pairs of vertebrate sister species. Consistent with the predictions of Janzen's climatic zonation hypothesis [9
], we found that the geographical distributions of tropical species encompass narrower thermal regimes than those of temperate species from the Northern Hemisphere in the New World. However, in contrast to recent studies on salamanders [17
] and frogs [20
], we found that sister species tend to exhibit a greater overlap in their thermal regimes in the tropics than in the temperate zone. Together, these results provide new insights on the evolutionary and biogeographic processes associated with the high species richness of tropical montane regions. Specifically, our study suggests that the thermal niches of tropical sister species tend to be narrower and more evolutionarily conserved than those of temperate sister species. As a result, populations may generally experience greater opportunities for isolation and allopatric speciation across elevational thermal gradients in tropical than in temperate montane regions.
Palaeontological and neontological studies have documented patterns of diversification consistent with the idea that rates of speciation are faster at lower latitudes (but see [30
], reviewed by [31
]). Some investigators have proposed that latitudinal variation in climatic zonation might contribute to this pattern by driving faster speciation in tropical montane organisms [12
]. However, it has remained unclear whether the greater climatic zonation of tropical mountains might promote speciation by increasing opportunities for allopatric isolation of populations with evolutionarily conserved thermal regimes, or by driving adaptive divergence of populations distributed along elevational climatic gradients [12
]. Based on our expanded sampling of vertebrate taxa, we find that thermal regimes of tropical sister species are generally more conserved than those of temperate ones, suggesting that the greater stability of temperature regimes along tropical mountain slopes could increase opportunities for isolation and allopatric speciation.
Of course, our results only indirectly support the idea that thermal tolerances of species are narrower and more evolutionarily conserved in tropical mountains relative to temperate ones. If species restrict the breadth of temperatures they experience by selecting appropriate microhabitats, regulating activity times or hibernating (especially at higher latitudes), then the use of macroclimatic data could overestimate the actual thermal tolerance breadths of species. However, the few studies that have systematically examined latitudinal variation in thermal tolerance have found a positive relationship between latitude, thermal regime breadth and thermal tolerance range [13
], although interspecific variation in thermal tolerance breadth increases with latitude as a result of the presence of species engaging in periods of extended inactivity [23
]. Thus, based on available evidence, our results do not appear to be driven by a greater mismatch between thermal regime breadths and thermal tolerance ranges in the temperate zone. Regardless, explicit tests of whether thermal regime, thermal tolerance, the thermal sensitivity of performance and the ability for thermal acclimation are correlated at geographical scales are sorely needed [35
Similarly, if biotic interactions (e.g. competition) limit the ranges of species [36
], then thermal regime widths inferred from geographical distribution data may encompass only a subset of the thermal conditions that species can tolerate. Although biotic interactions are generally thought to be stronger in the tropics [38
], there is some evidence to the contrary. For example, Huey [10
] found that the turnover of species along tropical versus temperate elevational gradients is unrelated to variation in the number of co-occurring species, a finding that contradicts the idea that competition plays a greater role in driving faunal turnover in the tropics. Likewise, in treefrogs, competition appears to play a role in community assembly in the temperate zone, but not in the tropics [39
]. It also seems unlikely that the latitudinal trends we document here are explained entirely by mismatches between the realized and fundamental thermal niches of species. First, given the stronger thermal gradients in tropical mountains, one would expect sister species to have divergent thermal niches, which is the exact opposite of the trend that we recovered. Second, interactions between species should reinforce any impacts of elevational climatic zonation on the physiological tolerances of species. For example, competitive interactions would be more likely to prevent a tropical than a temperate species from encountering a wide range of climatic conditions. Over evolutionary time, one might reasonably expect such pre-emptive occupation of geographical space to cause tropical species to become more physiologically specialized than temperate species. Thus, latitudinal patterns in thermal niche evolution may ultimately arise as a result of interactions between abiotic and biotic factors [19
In contrast to the predictions of Janzen's climatic zonation hypothesis and the results of a recent study that quantified vertebrate elevational range sizes across latitude [15
], we did not find that tropical species had narrower elevational extents than temperate species. However, we point out that patterns of thermal variation, rather than elevation per se
, formed the core of Janzen's idea. If species shift their elevational ranges locally to track preferred temperatures (e.g. moving to higher elevations at lower latitudes and vice versa
), then range-wide measures of elevational ranges (as we report here) are likely to provide a misleading proxy for the range of thermal conditions over which a species occurs [40
]. Previous studies focused on local transects or single mountains [9
] have not encountered this additional complexity, which may emerge when the ranges of elevations occupied by multiple populations of any given species are evaluated. Future studies should address whether populations of elevationally wide-ranging species show a greater propensity for local thermal adaptation in the tropics relative to the temperate zone (e.g. low seasonality in the tropics may enable local adaptation of physiology at small scales more readily).
Our inferences assume that the geographical and ecological contexts of speciation have not been obscured by regional differences (i.e. tropics versus temperate zones) in opportunities for post-speciational changes in the distributions of species. By including genetic distance between species as a covariate in analyses (a surrogate for the time available for post-speciation range shifts), we have attempted to reduce this potential source of error. Genetic distances did not vary significantly between temperate and tropical species in our dataset, suggesting that regional differences in the time available for species ranges to change in position and size [30
] do not explain the latitudinal trends that we found, although we note that the rate at which species distributions shift following speciation can vary with latitude [42
]. Further, we cannot rule out the possibility that species in both regions have shifted their elevational and climatic distributions since their formation in response to climate change, mountain uplift or species interactions [36
]. Nevertheless, it is difficult to envision how extensive post-speciation range shifts would result in a statistically significant, rather than random, pattern of the thermal overlap of tropical versus temperate sister species. Regardless, genetic studies of inter-population migration rates will be critical to further test the hypothesis that climatic gradients on mountains are stronger barriers to dispersal in the tropics compared with temperate systems.
Our results suggest that the thermal niches of tropical vertebrates are generally more conserved at the level of sister species than are those of temperate ones, a result consistent with a recent analysis focused on mammals using a different comparative approach [21
]. However, exactly why tropical species should exhibit greater conservatism of their thermal niches is unclear and will require further study. One possible explanation is that greater climatic stability in the tropics over time [46
] has promoted phylogenetic conservatism in the thermal niches of species. Alternatively, but non-exclusively, biotic interactions in the tropics could restrict the climatic distributions of lineages over time [47
Although our results suggest that climatic niches of vertebrate sister species are generally more conserved in the tropics than in the temperate zone, this pattern is not universal. For example, the narrower thermal tolerances of tropical plethodontid salamanders lead to a greater tendency for climatic niche divergence and speciation along elevational climatic gradients [17
]. In general, the greater climatic zonation of tropical mountains should increase opportunities for either allopatric or parapatric speciations. However, the extent to which such climatic zonation triggers speciation along elevational gradients may ultimately depend on the balance between dispersal and selection [48
]. Thus, one might predict that ecological speciation through climatic niche divergence along mountain slopes would be more prevalent in tropical taxa with the most limited dispersal abilities. Among the vertebrate taxa examined to date, plethodontid salamanders exhibit the most extreme spatial genetic structuring of populations [49
], suggesting that they are probably more dispersal-limited than birds, mammals, reptiles and anurans. Thus, differences in dispersal abilities might explain the different speciation patterns between plethodontids and other vertebrate taxa.
Taken together, and bearing in mind the potential shortcomings of exploring thermal regime variation from distributional data, our results suggest that tropical sister species exhibit greater evolutionary conservatism in their thermal niches than temperate sister species. Although numerous studies have documented dramatic differences in species richness and rates of diversification between the tropics and temperate zones, few have quantified, to the extent demonstrated here, how the interplay between climatic conditions, the evolution of species' niches and speciation might shape patterns of diversity. This work, we hope, will inspire more detailed examination of the physiological mechanisms that might underlie the patterns we document here, and whether and how they influence variation in speciation mechanisms among taxa and latitudes.