Evolutionary history of lagomorphs in response to global environmental change

Abstract

Although species within Lagomorpha are derived from a common ancestor, the distribution range and body size of its two extant groups, ochotonids and leporids, are quite differentiated. It is unclear what has driven their disparate evolutionary history. In this study, we compile and update all fossil records of Lagomorpha for the first time, to trace the evolutionary processes and infer their evolutionary history using mitochondrial genes, body length and distribution of extant species. We also compare the forage selection of extant species, which offers an insight into their future prospects. The earliest lagomorphs originated in Asia and later diversified in different continents. Within ochotonids, more than 20 genera occupied the period from the early Miocene to middle Miocene, whereas most of them became extinct during the transition from the Miocene to Pliocene. The peak diversity of the leporids occurred during the Miocene to Pliocene transition, while their diversity dramatically decreased in the late Quaternary. Mantel tests identified a positive correlation between body length and phylogenetic distance of lagomorphs. The body length of extant ochotonids shows a normal distribution, while the body length of extant leporids displays a non-normal pattern. We also find that the forage selection of extant pikas features a strong preference for C(3) plants, while for the diet of leporids, more than 16% of plant species are identified as C(4) (31% species are from Poaceae). The ability of several leporid species to consume C(4) plants is likely to result in their size increase and range expansion, most notably in Lepus. Expansion of C(4) plants in the late Miocene, the so-called 'nature's green revolution', induced by global environmental change, is suggested to be one of the major 'ecological opportunities', which probably drove large-scale extinction and range contraction of ochotonids, but inversely promoted diversification and range expansion of leporids.

Figure 1. Fossil occurrences of leporids and ochotonids shown alongside global environmental change.

A. Occurrences of genera in different epochs. The occurrences of ochotonids are updated from Ge et al. . Black bars give the extinct genera, green bars give the extant genera. The lengths of these bars are based on the maximum age and minimum age of each genus. B. The global climate change (Figure 2 in [110]) and vegetation change , and the genera number of ochotonids and leporids.

Figure 2. Fossil occurrences of ochotonids and leporids.

A, D, Eocene to Oligocene; B, E: Miocene; C, F: Pliocene to Holocene. Triangles show the occurrences of ochotonids, pentagons show the occurrence of leporids. Scale of 7000 miles is at the Equator.

Figure 3. Phylogenetic relationships and divergence times of Lagomorpha.

Branch labels on the tree give posterior probabilities. Node labels give median value of divergence time. Blue bars give 95% interval confidence of divergence time. Three ecotype groups of Ochotona are marked in different colors: red, the Mountain group; blue, the Northern group; pink, the shrub-steppe group.

Figure 4. The historical distribution of Lagomorpha inferred from different algorithms: S-DIVA, Bayes-DIVA, Maximum parsimony.

The phylogeny was based on the majority consensus trees derived from Bayesian inference analysis of three genes. Posterior probabilities are shown beside each node. Biogeographical regions used in the analysis including: Asia (A), Europe (B), North America (C), South America (D) and Africa (E). Out groups were excluded in the figures. Three methods identified Asia as the origin center of Lagomorpha (Node 1, S-DIVA 100%, Bayes-DIVA 79%, Maximum parsimony, 100%). Asia was also identified as the most probable ancestral region of leporids and ochotonids respectively (Node 2 and 3), while, Lepus firstly appeared in North America (Node 4).

Figure 5. Body size evolution in Lagomorpha.

The phylogenetic structure was based on Bayesian inferences. The body lengths of terminal taxa were mainly from PanTHERIA or calculated basing on museum collections. Body length of each node was inferred by parsimony methods. Colors on the branches show the change of body size. The units of body length are millimeters.

Figure 6. Frequency of log body length for extant ochotonids and leporids.

A. Ochotonids, this figure shows a slightly right skewed distribution, with a mode tending to smaller species. B. Leporids, this figure shows a left skewed distribution, with a mode tending to larger species.

Figure 7. Comparing forage selection of extant laghomorphs and other herbivores.

A. Forage selection of extant ochotonids, 63 families were reported as food (consumed directly or collected for hay piles) of extant ochotonids, these plant information mainly follows Ge et al. , which was summarized from 29 sources. B. Forage selection of leporids. 91 families were reported as food of leporids. These information was summarized from 28 sources. The top ten families selected by extant ochotonids and leporids are compared with the number of species and their proportions. C. Comparing C₃, C₄ and other components in the diet of different herbivores. 1. Ochotona curzoniae [Reference S29 in File S1], 2. Ochotona dauurica [Reference S29 in File S1], 3. Ochotona curzoniae [Reference S30 in File S1]; 4. Ochotona princeps [Reference S31 in File S1]; 5. Lepus timidus [Reference S32 in File S1]; 6. Lepus europaeus [Reference S33 in File S1]; 7. Lepus flavigularis [Reference S34 in File S1]; 8. Oryctolagus cuniculus [Reference S35 in File S1]; 9. Sylvilagus floridanus [Reference S36 in File S1]; 10. Sylvilagus auduboni [Reference S37 in File S1]; 11. Moschus berezovskii [Reference S38 in File S1]; 12. Pantholops hodgsoni [Reference S39 in File S1]; 13. Bos primigenius [Reference S40 in File S1]; 14. Ovis canadensis [Reference S40 in File S1]; 15. Equus africanus asinus [Reference S40 in File S1]; 16. Elaphurus davidianus [Reference S41 in File S1].Scale of 7000 miles is at the Equator.