A molecular timescale for caviomorph rodents (Mammalia, Hystricognathi)

Molecular Phylogenetics and Evolution 37 (2005) 932–937 www.elsevier.com/locate/ympev

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A molecular timescale for caviomorph rodents (Mammalia, Hystricognathi) Juan C. Opazo ¤ Center for Molecular Medicine and Genetics, School of Medicine, Wayne State University, Detroit, MI 48201, USA Received 8 February 2005; revised 3 May 2005 Available online 8 August 2005

1. Introduction Phylogenetic relationships and divergence times are important pieces of information for evolutionary biologists, given that they provide a framework for understanding the evolution of phenotypes. There are now statistical methods that estimate divergence times without assuming that all lineages evolve at the same rate (Huelsenbeck et al., 2000; Sanderson, 1997; Thorne et al., 1998). Here I apply these methods to the neotropical hystricomorph rodents. The hystricomorph rodents are highly diverse in terms of life history traits, body sizes, and overall reproductive strategies (Begall et al., 1999; ScharV et al., 1999). This diversity in life history strategies and body size is accompanied by considerable heterogeneity in rates of molecular evolution (Honeycutt et al., 2003; Huchon et al., 2000; Huchon and Douzery, 2001; Rowe and Honeycutt, 2002). The faster rate of molecular evolution of rodents compared to other mammals has been attributed to the shorter generation times of rodents (Gu and Li, 1993). However, the rate heterogeneity observed among hystricognath rodents suggests that the causes of rate heterogeneity may be more complex than previously thought (Gu and Li, 1993). Huchon and Douzery (2001) have addressed the problem of divergence times among major clades of hystricomorph rodents. Others have estimated divergence times using more complex taxonomic sampling for speciWc groups such as the caviomorph rodents (neotropical hystricomorph rodents) (Galewski et al., 2005; Honeycutt et al., 2003). Among these rodents, the superfamily Octo-

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dontoidea deserves special attention because of the extensive radiations of the members of its families Ctenomyidae (tuco-tucos) and Echimyidae (spiny rats) (Galewski et al., 2005; Lessa and Cook, 1998). Also within the family Octodontidae there are two tetraploid species (Tympanoctomys barrerae and Pipanoctomys aureus) that appear to be sister groups (Gallardo et al., 1999, 2004); nevertheless, there are no estimations regarding when the two species last shared a common ancestor. The objective of this work is to reevaluate divergence times within caviomorph rodents using a new statistical methodology, a better phylogenetic relationship hypothesis, and a widespread taxonomic sample that includes all of the major groups of caviomorph rodents.

2. Materials and methods Sequences of the growth hormone receptor and 12S ribosomal RNA gene were obtained from GenBank for 33 caviomorph (South American group) and 3 phiomorph (African group) species (Table 1). Ctenodactylus gundi was used as an outgroup. Divergence times were estimated using MULTIDIVTIME software (Kishino et al., 2001; Thorne et al., 1998). Parameter estimation for each gene was obtained using the BASEML module of the PAML package (Yang, 1997). Branch lengths and the variance–covariance matrixes were estimated using ESTBRANCHES. To estimate divergence times, the Markov chain was sampled 200,000 times every 5 cycles, after a burnin of 2,000,000 cycles. The number of time units between the root and the tip of the tree was 55 Myr, however, I forced the time units (rttime) to be 2, according to Thorne’s

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Table 1 Species names, family and accession numbers for GHR and 12S genes Species name

Family

GHR

12S

Abrocoma cinerea Agouti paca Agouti taczanowskii Heterocephalus glaber Cavia aperea Cavia porcellus Dolichotis patagonum Dolichotis salinicola Galea musteloides Galea spixii Kerodon rupestris Microcavia australis Chinchilla lanigera Ctenodactylus gundi Ctenomys steinbachi Dasyprocta punctata Myoprocta acouchy Myoprocta pratty Dinomys branickii Hoplomys gymnurus Proechimys longicaudatus Erethizon dorsatum Hydrochaeris hydrochaeris Hystrix africaeaustralis Myocastor coypus Aconaemys fuscus Aconaemys porteri Aconaemys sagei Octodon bridgesi Octodon degus Octodon lunatus Octodontomys gliroides Octomys mimax Pipanoctomys aureus Spalacopus cyanus Tympanoctomys barrerae Thryonomys swinderianus

Abrocomidae Agoutidae Agoutidae Bathyergidae Caviidae Caviidae Caviidae Caviidae Caviidae Caviidae Caviidae Caviidae Chinchillidae Ctenodactylidae Ctenomyidae Dasyproctidae Dasyproctidae Dasyproctidae Dinomyidae Echimyidae Echimyidae Erethizontidae Hydrochaeridae Hystricidae Myocastoridae Octodontidae Octodontidae Octodontidae Octodontidae Octodontidae Octodontidae Octodontidae Octodontidae Octodontidae Octodontidae Octodontidae Thryonomyidae

AF520643 AF433928 AF433929 AF332034 AF433930 AF433931 AF433939 AF433941 AF433933 AF433935 AF433938 AF433937 AF520660 AF332042 AF520656 AF433943 AF433945 AF433946 AF332038 AF520661 AF332039 AF332037 AF433948 AF332033 AF520662 AF520657 AF520644 AF520645 AF520646 AF520647 AF520651 AF520664 AF520665 AY249752 AF520654 AF520655 AF332035

AF520666 AF433906 AF433907 AY425847 AF433908 NC000884 AY093662 AF433918 AF433910 AF433912 AY765988 AY765989 AF520696 U67301 AF520667 AF433921 AF433922 AF433923 AF520697 AF520668 PLU12447 AF520694 AF433925 HAU12448 AF520669 AF520675 AF520670 AF520673 AF520677 AF520680 AF520682 AF520685 AF520687 AY249753 AF520690 AF520692 NC002658

recommendation. The rtrate ( D rtratesd) value was set by calculating the median value of the amount of evolution from the root to the tip of the tree, and averaging this value for both genes (JeV Thorne, pers. comm.). To check the consistency of the results, I ran the program using all three values. Brownmean ( D brownsd) was 0.5. I chose 65 Myr as the highest possible amount of time between the tip and root. I used caviomorph radiation at 31–37 Mya as the calibration point. This calibration point was chosen based on the appearance of the Wrst caviomorph fossil during the Tinguirirican (Wyss et al., 1993), and to assure that the results were comparable with other estimations.

3. Results and discussion Divergence times between the families Bathyergidae (represented by Heterocephalus glaber) and Thryonomyidae (represented by Thryonomys swinderianus), and

the Caviomorpha–Phiomorpha split (Fig. 1) were younger than the estimations reported by Huchon and Douzery (2001) and Sarich (1985), but the divergence time for the Caviomorpha/Phiomorpha split was older than the estimation reported by Wood (1985). The crown group of Caviomorph rodents was dated 33.8 § 1.8 Mya (Fig. 1), which is more compatible with the estimation of 32.2 § 2.4 Mya reported by Galewski et al. (2005), than the value of 35–40.4 Mya reported by Honeycutt et al. (2003) (Table 2). Based on the fossil record, Vucetich et al. (1999) recognize two main radiations in the Caviomorph group; According to these authors the Wrst radiation occurred during the Eocene–Oligocene boundary (t33 Mya). In contrast, Huchon and Douzery (2001) report that this radiation occurred during the middle-late Oligocene (t23.8–30 Mya). Here, I estimate an intermediate date for the radiation event at superfamilial level during the early Oligocene (28.5–33.7 Mya) (Fig. 1). The crown group of the superfamily Cavioidea was estimated at 27.9 § 2.4 Mya (Fig. 1); this value is older

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Fig. 1. Divergence time estimates for Caviomorph rodents using a relaxed molecular clock. Each value represents the divergence time in millions of years § SD. Caviomorph radiation at 31–37 Mya was used as the calibration point (Wyss et al., 1993). Geological times are reported according to the 1999 Geologic Time Scale of the Geological Society of America (PP, Plio-Pleistocene). At superfamilial level phylogenetic relationships were obtained from Huchon and Douzery (2001); for members of the superfamily Cavioidea from Rowe and Honeycutt (2002); for members of the superfamily Octodontoidea from Honeycutt et al. (2003); and for members of the family Echimyidae from Galewski et al. (2005).

than the estimated value of 21–26 Mya by Huchon and Douzery (2001) (Table 2). The second major radiation of Caviomorph rodents proposed by Vucetich et al. (1999), took place in the middle-late Miocene. In accordance with these authors here I estimate the main diversiWcation of the superfamily Cavioidea in the middle-late Miocene (Fig. 1), however the value I obtained is younger than the early Miocene estimation proposed by Huchon and Douzery (2001). Nevertheless, it is important to note that these estimations were made using more species, and slightly diVerent phylogenetic relationships than in the study by Huchon and Douzery (2001). Furthermore, since Cavioidea rodents comprise diverse kinds of breeding systems, degrees of sociality, body sizes, gestation times, habitat use, and other traits (Rowe and Honeycutt, 2002), these results represent an advance for understanding the evolution of these phenotypes. In cases where two species of the same genus were analyzed, the mean diver-

gence was 5.1 Mya, this result agrees with the idea of a time-based classiWcation, in which an age younger than 6 Mya should be indicative of members of the same genus (Goodman et al., 1998). Similar results were obtained in the family Echimyidae (Galewski et al., 2005). According to this study, as well as the work by Huchon and Douzery (2001), the split of Erethizontoidea and Chinchilloidea+Octodontoidea took place in the early Oligocene (Fig. 1) (Table 2). The splitting of Chinchilloidea and Octodontoidea also would have occurred in the early Oligocene (Fig. 1), which is older than the late Oligocene estimation by Huchon and Douzery (2001) (Table 2). The interesting clustering of Chinchillidae and Dinomyidae found by Huchon and Douzery (2001) was recently validated by Spotorno et al. (2004). In agreement with previous estimations (Table 2), this study indicates that the divergence between Dinomys and Chinchilla occurred during the early Miocene (Fig. 1).

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Table 2 Comparison of the divergence times found in this study with values from previously published articles This study Stem Caviomorph Stem Cavioidea Stem Chinchilloidea Stem Octodontoidea Cavia/Hydrochaeris Eretdea/Chindea+Ocdea Chindea/Ocdea Chin/Dino Echdae/Ctenodae+Ocdae Ctenodae/Ocdae Stem Octodontidae Oglir/Octodon+Spa+Aco Octodon/Aco+Spa

33.8 § 1.8 27.9 § 2.4 19.1 § 2.7 20.6 § 2.4 18.5 § 2.5 32.9 § 1.8 31.4 § 2.0 19.1 § 2.7 17.5 § 2.2 15 § 2.1 7.79 § 1.5 6.07 § 1.3 3.69 § 0.9

Huchon and Douzery (2001)

Galewski et al. (2005)

Honeycutt| et al. (2003)

Gallardo and Kirsch (2001)

— 21–26 17–21 15–18 14–17 29–31 25–29 17–21 — — — — —

32.2 § 2.4 — — — — — — — 22.4 § 3.9 — — — —

35–40.4 — — — — — — — 23.1–31.6 16.7–22.5 5–14.1 2.9–4.1 1.1–5.3

— — — 25–30 — — 35–37 — — 25 7–10 5–7 4–5

Eretdea, superfamily Erethizontoidea; Chindea, superfamily Chinchilloidea; Ocdea, superfamily Octodontoidea; Chin, Chinchilla lanigera; Dino, Dinomys branickii; Echdae, family Echimyidae; Ctenodae, family Ctenomyidae; Ocdae, family Octodontidae; Oglir, Octodontomys gliroides; Spa, Spalacopus cyanus; Aco, genus Aconaemys.

Fig. 2. Divergence time estimates for members of the family Octodontidae using a relaxed molecular clock. Each value represents the divergence time in millions of years § SD. T. barrerae and P. aureus represent the two tetraploid species. Geological times are reported according to the 1999 Geologic Time Scale of the Geological Society of America. Phylogenetic relationships were obtained from Gallardo et al. (2004).

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Since the branch pattern used in Huchon and Douzery (2001) to estimate divergence times among members of the superfamily Octodontoidea was diVerent than in my study, our results are not directly comparable. Nevertheless, it is possible to make some general comparisons. First, in agreement with these authors, radiation at the familial level occurred during the Miocene (Fig. 1). The crown group of the superfamily Octodontoidea was dated during the early Miocene (20.6 § 2.4 Mya), which is a little older than the estimation made by Huchon and Douzery (2001) (Table 2). Using DNA hybridization, Gallardo and Kirsch (2001) dated this point between 25–30 Mya (Table 2). According to this study, the next split (Echimyidae and Ctenomyidae+Octodontidae) occurred 17.5 § 2.2 Mya (Fig. 1), which is younger than that estimated by Honeycutt et al. (2003), but within the range according to Galewski et al. (2005) (Table 2). In this study, the divergence of Myocastor and Echimyidae, and both spiny rat species are estimated to have occurred around 8.6 § 1.7 and 5.6 § 1.3 Mya (Fig. 1), respectively. The divergence between Ctenomyidae and Octodontidae was estimated to have occurred during the middle Miocene, around 15 § 2.1 Mya (Fig. 1), which is younger than the estimations made by Gallardo and Kirsch (2001) and Honeycutt et al. (2003) (Table 2). The divergence times for the family Octodontidae obtained from this study are of great interest since this work includes almost all of the species of the family, as well as the presence of the two tetraploid species (Gallardo et al., 1999, 2004). According to these results, the main diversiWcation of the family Octodontidae occurred in the Plio-Pleistocene (Fig. 2), which is coincident with changes in the landscape and habitat fragmentation (Honeycutt et al., 2003). The crown of the family Octodontidae was estimated in the late Miocene, around 7.79 § 1.55 Mya (Fig. 2), this value falls between the estimation made by Honeycutt et al. (2003) and the estimation based on DNA hybridization (Gallardo and Kirsch, 2001) (Table 2). Furthermore, the split of Octomys mimax and the two tetraploid species (Tympanoctomys barrerae+Pipanoctomys aureus) would have occurred in the Pliocene, around 4.28 § 1.08 Mya (Fig. 2), which is more recent than the late Miocene estimation of t6.5 Mya using DNA hybridization (Gallardo and Kirsch, 2001). More interesting is the divergence of the two tetraploid species, T. barrerae and P. aureus, which, according to this work, occurred in the Plio-Pleistocene boundary t1.74 § 0.59 Mya (Fig. 2). The divergence of Octodontomys gliroides and Octodon+Spalacopus+Aconaemys genera would have occurred during the late Miocene, around 6.07 § 1.34 Mya (2). This value is in agreement with the estimation based on DNA hybridization (Gallardo and Kirsch, 2001), but is older than the estimation of Honeycutt et al., 2003) (Table 2). Divergence between the genera Octodon, Spalacopus, and

Aconaemys, as well as within each group, occurred during the Plio-Pleistocene (Fig. 2) (Table 2), which is in agreement with previous estimations (Gallardo and Kirsch, 2001; Honeycutt et al., 2003). Acknowledgments The author thank Drs. Morris Goodman and Lawrence Grossman for computer facilities and JeV Thorne for his assistance with the software. I also thank two anonymous reviewers for their comments.

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