Recurrent cycles of climatic change during the Quaternary period have dramatically affected the population genetic structure of many species. We reconstruct the recent demographic history of the coyote (Canis latrans) through the use of Bayesian techniques to examine the effects of Late Quaternary climatic perturbations on the genetic structure of a highly mobile generalist species. Our analysis reveals a lack of phylogeographic structure throughout the range but past population size changes correlated with climatic changes. We conclude that even generalist carnivorous species are very susceptible to environmental changes associated with climatic perturbations. This effect may be enhanced in coyotes by interspecific competition with larger carnivores.
The Pleistocene was characterized by recurrent climatic perturbations resulting in dramatic environmental changes that affected the distribution and population structure of plants and animals . In temperate species, glacial periods were generally associated with range reductions owing to restriction of habitat, whereas interglacial periods were typically associated with range expansion. Many taxa illustrate the effects such climate changes had on phylogeographic and demographic patterns . In particular, the last glacial–interglacial transition coincided with major extinction events and population declines in numerous species distributed in the Northern Hemisphere [1,3]. In contrast, distribution and phylogeographic patterns from other organisms were amplified by the process of colonization of newly available habitat after the last glacial maximum [2,4] and basic patterns in the routes of post-glacial expansions have emerged .
The degree of habitat specialization is likely to affect the ability of species to persist during rapid environmental changes, and specialist species had a higher risk of extinction during the Pleistocene . Generalist species, on the other hand, are more likely to survive because a subset of habitats allowing their existence remains throughout climate fluctuations. To examine the role of Late Pleistocene and Holocene climatic changes in shaping the genetic structure of a highly mobile generalist carnivore, we inferred the phylogeographic structure and demographic history of the coyote, Canis latrans, in North America based on sequences of the mitochondrial control region.
2. Material and methods
Our study is based on 837 sequences of a 414 bp fragment (including gaps) of the mitochondrial control region from coyote samples spanning the entire current distribution in the US and Canada (electronic supplementary material, table S1). To visualize the phylogenetic relationships among the coyote haplotypes, we conducted a Bayesian phylogenetic analysis using MrBayes v. 3.1.2 . Spatial genetic structure of coyotes was analysed by spatial analysis of molecular variance using SAMOVA v. 1.0 . To test for signals of population expansion, we calculated a mismatch distribution and conducted two neutrality tests (Tajima's D, Fu's Fs). We excluded samples from the most recently (last century) colonized eastern North America because recurrent gene flow between the invading coyotes and resident eastern wolves [9–11] might bias demographic inferences. Past population size trajectories were inferred using a Bayesian coalescent (Bayesian Skyline Plot, BSP ) approach as implemented in BEAST v. 1.5.4 . To estimate absolute ages of demographic events, we applied a substitution rate of 4.68 (and additionally 9.36 and 3.64) per cent per million years which is based on an average sequence divergence of 13.1 per cent  and the estimated split between coyotes and gray wolves 1.4 (0.7–1.8) Myr . A detailed description of the analytical procedure is given in the electronic supplementary material.
3. Results and discussion
Regional phylogeographic structure was neither detected in our Bayesian phylogenetic analysis (figure 1; cf. ) nor in our spatial analysis of molecular variance (electronic supplementary material, figure S1) which is consistent with a lack of a strong population structure on a continental scale [11,16]. Given that (i) coyotes are good dispersers (individual dispersal distances over 100 km have been reported ), (ii) they are highly adaptable to different resources and (iii) their natural distribution range (the grasslands of the Great Plains) was not fragmented during the Late Pleistocene glacial cycles, then their population genetic structure is expected to be low. However, the lack of a clear phylogeographic structure across the coyote's entire distribution is quite remarkable and rather unusual among North American mammals. Most larger mammals that survived the Last Glacial Maximum (LGM) in North America and now inhabit a large part of the continent show a distinct phylogeographic pattern consistent with survival at reduced population sizes in two or more isolated, ice-free refugia [18–21]. A similar pattern has been reported on a continental scale in the closely related gray wolf . On small geographic scales, habitat-associated population partitions have been observed both in coyotes  and gray wolves [9,23,24].
Mismatch distribution (figure 2a) and neutrality tests (D = −1.4423, p = 0.036; Fs = −23.8241, p = 0.006) reject a constant population size through time. The pattern of past population size trajectories, as inferred by BSP, corresponds with environmental and climatic fluctuations in the Late Pleistocene (figure 2b). Population declines might be difficult to infer based solely on contemporary samples, and BSP patterns might be indistinguishable from constant population size through time. However, this should not be true for periods of rapid population growth. It is probable that the inferred population expansions followed periods of reduced population sizes, something impossible to infer with just contemporaneous data, in particular when it concerns events far in the past. Our analysis inferred a population expansion at the penultimate (Illinoian–Sangamonian) glacial–interglacial transition, which was likely facilitated by an associated change of the environment from forested habitats in the Illinoian to more open country in the Sangamonian . Cooling climate and associated vegetation changes during the Late Wisconsinian glacial, in particular the spread of forests in the northern plains region , coincides with a population decline with a minimum after the last glacial maximum (approx. 20 kyr), regardless of the substitution rate used (figure 2b, electronic supplementary material, figure S2). Thereafter, the spread of grasslands in the Holocene approximately 9.5–5 kyr (depending upon location)  is associated with a drastic population expansion of coyotes. This expansion peaked in the recent rapid colonization of nearly the entire North American continent. However, this recent colonization may have been facilitated by the near extermination of an interference competitor, the gray wolf, in large parts of North America  and changes in the landscape owing to the spread of agriculture. Moreover, as coyotes generally avoid dense woodland habitats, their colonization of such habitats in the North American northeast might have been facilitated by hybridization with ‘eastern’ wolves [12,13]. Today, coyotes are found throughout North America in a variety of habitats, except the High Arctic.
Recent evidence suggests a potentially time-dependent rate of molecular evolution, which could affect the dating of recent evolutionary/demographic events, in particular, if one applies a molecular rate obtained from an ancient split to more recent events . However, even if our estimates were affected by this phenomenon they would be biased towards older ages. This implies that the population decline observed in the BSP by all means post-dates the LGM.
In conclusion, high dispersal distances and adaptability to different resources are likely to have contributed to the lack of large-scale phylogeographic structuring found in this study. However, although coyotes are a generalist species that can exist in a wide range of habitat types and feed on various kinds of prey, the coyote experienced demographic changes that correlate with the Late Quaternary expansion and contraction of dry grasslands. Only recently, with the local extermination of wolves, habitat changes and local hybridization with ‘eastern’ wolves, have coyotes been able to colonize a greater diversity of habitats. The combined effects of interspecific competition and climate change have likely driven demographic changes in coyotes throughout their evolutionary history.
We thank all of the many individuals and agencies that assisted in sample collection. This project was supported by the Swedish Research Council, Carl Tryggers Foundation, CSIC, Programa de Captación del Conocimiento para Andalucía (Spain) and NSF (DEB 0733033).
- Received February 25, 2012.
- Accepted March 7, 2012.
- This journal is © 2012 The Royal Society