A Molecular Timescale for Caviomorph Rodents (Mammalia, Hystricognathi)

Home , Abrocoma, Hystricognathi, Phiomorpha

Molecular Phylogenetics and Evolution 37 (2005) 932–937 www.elsevier.com/locate/ympev Short communication 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 dontoidea deserves special attention because of the extensive radiations of the members of its families Phylogenetic relationships and divergence times are Ctenomyidae (tuco-tucos) and Echimyidae (spiny rats) important pieces of information for evolutionary biolo- (Galewski et al., 2005; Lessa and Cook, 1998). Also gists, given that they provide a framework for under- within the family Octodontidae there are two tetraploid standing the evolution of phenotypes. There are now species (Tympanoctomys barrerae and Pipanoctomys statistical methods that estimate divergence times with- aureus) that appear to be sister groups (Gallardo et al., out assuming that all lineages evolve at the same rate 1999, 2004); nevertheless, there are no estimations (Huelsenbeck et al., 2000; Sanderson, 1997; Thorne et al., regarding when the two species last shared a common 1998). Here I apply these methods to the neotropical ancestor. hystricomorph rodents. The hystricomorph rodents are The objective of this work is to reevaluate divergence highly diverse in terms of life history traits, body sizes, times within caviomorph rodents using a new statistical and overall reproductive strategies (Begall et al., 1999; methodology, a better phylogenetic relationship hypoth- ScharV et al., 1999). This diversity in life history strate- esis, and a widespread taxonomic sample that includes gies and body size is accompanied by considerable heter- all of the major groups of caviomorph rodents. ogeneity 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 2. Materials and methods molecular evolution of rodents compared to other mam- mals has been attributed to the shorter generation times Sequences of the growth hormone receptor and 12S of rodents (Gu and Li, 1993). However, the rate hetero- ribosomal RNA gene were obtained from GenBank for geneity observed among hystricognath rodents suggests 33 caviomorph (South American group) and 3 phi- that the causes of rate heterogeneity may be more com- omorph (African group) species (Table 1). Ctenodactylus plex than previously thought (Gu and Li, 1993). Huchon gundi was used as an outgroup. and Douzery (2001) have addressed the problem of Divergence times were estimated using MULTIDIV- divergence times among major clades of hystricomorph TIME software (Kishino et al., 2001; Thorne et al., rodents. Others have estimated divergence times using 1998). Parameter estimation for each gene was obtained more complex taxonomic sampling for speciWc groups using the BASEML module of the PAML package such as the caviomorph rodents (neotropical hys- (Yang, 1997). Branch lengths and the variance–covari- tricomorph rodents) (Galewski et al., 2005; Honeycutt ance matrixes were estimated using ESTBRANCHES. et al., 2003). Among these rodents, the superfamily Octo- 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 * Fax: + 313 577 5218. root and the tip of the tree was 55 Myr, however, I forced E-mail address: [email protected]. the time units (rttime) to be 2, according to Thorne’s

Table 1 Species names, family and accession numbers for GHR and 12S genes Species name Family GHR 12S Abrocoma cinerea Abrocomidae AF520643 AF520666 Agouti paca Agoutidae AF433928 AF433906 Agouti taczanowskii Agoutidae AF433929 AF433907 Heterocephalus glaber Bathyergidae AF332034 AY425847 Cavia aperea Caviidae AF433930 AF433908 Cavia porcellus Caviidae AF433931 NC000884 Dolichotis patagonum Caviidae AF433939 AY093662 Dolichotis salinicola Caviidae AF433941 AF433918 Galea musteloides Caviidae AF433933 AF433910 Galea spixii Caviidae AF433935 AF433912 Kerodon rupestris Caviidae AF433938 AY765988 Microcavia australis Caviidae AF433937 AY765989 Chinchilla lanigera Chinchillidae AF520660 AF520696 Ctenodactylus gundi Ctenodactylidae AF332042 U67301 Ctenomys steinbachi Ctenomyidae AF520656 AF520667 Dasyprocta punctata Dasyproctidae AF433943 AF433921 Myoprocta acouchy Dasyproctidae AF433945 AF433922 Myoprocta pratty Dasyproctidae AF433946 AF433923 Dinomys branickii Dinomyidae AF332038 AF520697 Hoplomys gymnurus Echimyidae AF520661 AF520668 Proechimys longicaudatus Echimyidae AF332039 PLU12447 Erethizon dorsatum Erethizontidae AF332037 AF520694 Hydrochaeris hydrochaeris Hydrochaeridae AF433948 AF433925 Hystrix africaeaustralis Hystricidae AF332033 HAU12448 Myocastor coypus Myocastoridae AF520662 AF520669 Aconaemys fuscus Octodontidae AF520657 AF520675 Aconaemys porteri Octodontidae AF520644 AF520670 Aconaemys sagei Octodontidae AF520645 AF520673 Octodon bridgesi Octodontidae AF520646 AF520677 Octodon degus Octodontidae AF520647 AF520680 Octodon lunatus Octodontidae AF520651 AF520682 Octodontomys gliroides Octodontidae AF520664 AF520685 Octomys mimax Octodontidae AF520665 AF520687 Pipanoctomys aureus Octodontidae AY249752 AY249753 Spalacopus cyanus Octodontidae AF520654 AF520690 Tympanoctomys barrerae Octodontidae AF520655 AF520692 Thryonomys swinderianus Thryonomyidae AF332035 NC002658 recommendation. The rtrate ( D rtratesd) value was set the Caviomorpha–Phiomorpha split (Fig. 1) were youn- by calculating the median value of the amount of evolu- ger than the estimations reported by Huchon and tion from the root to the tip of the tree, and averaging Douzery (2001) and Sarich (1985), but the divergence this value for both genes (JeV Thorne, pers. comm.). To time for the Caviomorpha/Phiomorpha split was older check the consistency of the results, I ran the program than the estimation reported by Wood (1985). using all three values. Brownmean ( D brownsd) was 0.5. The crown group of Caviomorph rodents was dated I chose 65 Myr as the highest possible amount of time 33.8§1.8 Mya (Fig. 1), which is more compatible with the between the tip and root. I used caviomorph radiation at estimation of 32.2§2.4 Mya reported by Galewski et al. 31–37 Mya as the calibration point. This calibration (2005), than the value of 35–40.4Mya reported by Honey- point was chosen based on the appearance of the Wrst cutt et al. (2003) (Table 2). Based on the fossil record, caviomorph fossil during the Tinguirirican (Wyss et al., Vucetich et al. (1999) recognize two main radiations in the 1993), and to assure that the results were comparable Caviomorph group; According to these authors the Wrst with other estimations. radiation occurred during the Eocene–Oligocene boundary (t33Mya). In contrast, Huchon and Douzery (2001) report that this radiation occurred during the middle-late 3. Results and discussion Oligocene (t23.8–30Mya). Here, I estimate an intermedi- ate date for the radiation event at superfamilial level dur- Divergence times between the families Bathyergidae ing the early Oligocene (28.5–33.7Mya) (Fig. 1). (represented by Heterocephalus glaber) and Thryono- The crown group of the superfamily Cavioidea was myidae (represented by Thryonomys swinderianus), and estimated at 27.9 § 2.4Mya (Fig. 1); this value is older 934 J.C. Opazo / Molecular Phylogenetics and Evolution 37 (2005) 932–937

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 gence was 5.1 Mya, this result agrees with the idea of a Douzery (2001) (Table 2). The second major radiation of time-based classiWcation, in which an age younger than Caviomorph rodents proposed by Vucetich et al. (1999), 6 Mya should be indicative of members of the same genus took place in the middle-late Miocene. In accordance (Goodman et al., 1998). Similar results were obtained in with these authors here I estimate the main diversiWcation the family Echimyidae (Galewski et al., 2005). of the superfamily Cavioidea in the middle-late Miocene According to this study, as well as the work by (Fig. 1), however the value I obtained is younger than the Huchon and Douzery (2001), the split of Erethizontoidea early Miocene estimation proposed by Huchon and and Chinchilloidea+Octodontoidea took place in the Douzery (2001). Nevertheless, it is important to note that early Oligocene (Fig. 1) (Table 2). The splitting of Chin- these estimations were made using more species, and chilloidea and Octodontoidea also would have occurred slightly diVerent phylogenetic relationships than in the in the early Oligocene (Fig. 1), which is older than the late study by Huchon and Douzery (2001). Furthermore, Oligocene estimation by Huchon and Douzery (2001) since Cavioidea rodents comprise diverse kinds of breed- (Table 2). The interesting clustering of Chinchillidae and ing systems, degrees of sociality, body sizes, gestation Dinomyidae found by Huchon and Douzery (2001) was times, habitat use, and other traits (Rowe and Honeycutt, recently validated by Spotorno et al. (2004). In agreement 2002), these results represent an advance for understand- with previous estimations (Table 2), this study indicates ing the evolution of these phenotypes. In cases where two that the divergence between Dinomys and Chinchilla species of the same genus were analyzed, the mean diver- occurred during the early Miocene (Fig. 1). J.C. Opazo / Molecular Phylogenetics and Evolution 37 (2005) 932–937 935

Table 2 Comparison of the divergence times found in this study with values from previously published articles This study Huchon and Galewski et al. (2005) Honeycutt| Gallardo and Douzery (2001) et al. (2003) Kirsch (2001) Stem Caviomorph 33.8 § 1.8 — 32.2 § 2.4 35–40.4 — Stem Cavioidea 27.9 § 2.4 21–26 — — — Stem Chinchilloidea 19.1 § 2.7 17–21 — — — Stem Octodontoidea 20.6 § 2.4 15–18 — — 25–30 Cavia/Hydrochaeris 18.5 § 2.5 14–17 — — — Eretdea/Chindea+Ocdea 32.9 § 1.8 29–31 — — — Chindea/Ocdea 31.4 § 2.0 25–29 — — 35–37 Chin/Dino 19.1 § 2.7 17–21 — — — Echdae/Ctenodae+Ocdae 17.5 § 2.2 — 22.4 § 3.9 23.1–31.6 — Ctenodae/Ocdae 15 § 2.1 — — 16.7–22.5 25 Stem Octodontidae 7.79 § 1.5 — — 5–14.1 7–10 Oglir/Octodon+Spa+Aco 6.07 § 1.3 — — 2.9–4.1 5–7 Octodon/Aco+Spa 3.69 § 0.9 — — 1.1–5.3 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 Geo- logic Time Scale of the Geological Society of America. Phylogenetic relationships were obtained from Gallardo et al. (2004). 936 J.C. Opazo / Molecular Phylogenetics and Evolution 37 (2005) 932–937

Since the branch pattern used in Huchon and Aconaemys, as well as within each group, occurred Douzery (2001) to estimate divergence times among during the Plio-Pleistocene (Fig. 2) (Table 2), which is in members of the superfamily Octodontoidea was diVerent agreement with previous estimations (Gallardo and than in my study, our results are not directly compara- Kirsch, 2001; Honeycutt et al., 2003). ble. Nevertheless, it is possible to make some general comparisons. First, in agreement with these authors, radiation at the familial level occurred during the Acknowledgments Miocene (Fig. 1). The crown group of the superfamily Octodontoidea was dated during the early Miocene The author thank Drs. Morris Goodman and V (20.6 § 2.4 Mya), which is a little older than the estima- Lawrence Grossman for computer facilities and Je tion made by Huchon and Douzery (2001) (Table 2). Thorne for his assistance with the software. I also thank Using DNA hybridization, Gallardo and Kirsch (2001) two anonymous reviewers for their comments. 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 References (Fig. 1), which is younger than that estimated by Honey- cutt et al. (2003), but within the range according to Begall, S., Burda, H., Gallardo, M.H., 1999. Reproduction, postnatal Galewski et al. (2005) (Table 2). In this study, the diver- development, and growth of social coruros, Spalacopus cyanus (Rodentia: Octodontidae), from Chile. J. Mamm. 80, 210–217. gence of Myocastor and Echimyidae, and both spiny rat Galewski, T., MauVrey, J.-F., Leite, Y.L.R., Patton, J.L., Douzery, species are estimated to have occurred around 8.6 § 1.7 E.J.P., 2005. Ecomorphological diversiWcation among South Ameri- and 5.6 § 1.3 Mya (Fig. 1), respectively. The divergence can spiny rats (Rodentia; Echimyidae): a phylogenetic and chrono- between Ctenomyidae and Octodontidae was estimated logical approach. Mol. Phylogenet. Evol. 34, 601–615. to have occurred during the middle Miocene, around Gallardo, M.H., Bickham, J.W., Honeycutt, R.L., Ojeda, R., Köhler, N., § 1999. Discovery of tetraploidy in a mammal. Nature 401, 341. 15 2.1 Mya (Fig. 1), which is younger than the Gallardo, M.H., Kirsch, J.A.W., 2001. Molecular relationships among estimations made by Gallardo and Kirsch (2001) and octodontidae (Mammalia: Rodentia: Caviomorpha). J. Mamm. Honeycutt et al. (2003) (Table 2). Evol. 8, 73–89. The divergence times for the family Octodontidae Gallardo, M.H., Kausel, G., Jiménez, A., Bacquet, C., González, C., obtained from this study are of great interest since this Figueroa, J., Köhler, N., Ojeda, R., 2004. Whole-genome duplica- tions in South American desert rodents (Octodontidae). Biol. J. work includes almost all of the species of the family, as Linn. Soc. 82, 443–451. well as the presence of the two tetraploid species Goodman, M., Porter, C.A., Czelusniak, J., Page, S.L., Schneider, H., (Gallardo et al., 1999, 2004). According to these results, Shoshani, J., Gunnell, G., Groves, C.P., 1998. Toward a phyloge- the main diversiWcation of the family Octodontidae netic classiWcation of primates based on DNA evidence comple- occurred in the Plio-Pleistocene (Fig. 2), which is coinci- mented by fossil evidence. Mol. Phylogenet. Evol. 9, 585–598. Gu, X., Li, W.-H., 1993. Higher rates of amino acid substitution in dent with changes in the landscape and habitat fragmen- rodents than in humans. Mol. Phylogen. Evol. 1, 211–214. tation (Honeycutt et al., 2003). The crown of the family Honeycutt, R.L., Dowe, D.L., Gallardo, M.H., 2003. Molecular system- Octodontidae was estimated in the late Miocene, around atics of the South American Caviomorph rodents: relationships 7.79§1.55 Mya (Fig. 2), this value falls between the among species and genera in the family Octodontidae. Mol. Phylo- estimation made by Honeycutt et al. (2003) and the esti- genet. Evol. 26, 476–489. Huchon, D., CatzeXis, F.M., Douzery, E.J.P., 2000. Variance of molecu- mation based on DNA hybridization (Gallardo and lar datings, evolution of rodents and phylogenetic aYnities between Kirsch, 2001) (Table 2). Furthermore, the split of Octomys Ctenodactylidae and Hystricognathi. Proc. R. Soc. Lond. B. 267, mimax and the two tetraploid species (Tympanoctomys 393–402. barrerae+Pipanoctomys aureus) would have occurred in Huchon, D., Douzery, E.J.P., 2001. From the Old World to the New the Pliocene, around 4.28§1.08Mya (Fig. 2), which is World: A molecular chronicle of the phylogeny and biogeography t of Hystricognath rodents. Mol. Phylogenet. Evol. 20, 238–251. more recent than the late Miocene estimation of 6.5 Mya Huelsenbeck, J.P., Larget, B., SwoVord, D.L., 2000. A compound Pois- using DNA hybridization (Gallardo and Kirsch, 2001). son process for relaxing the molecular clock. Genetics 154, 1879– More interesting is the divergence of the two tetraploid 1892. species, T. barrerae and P. aureus, which, according to this Kishino, H., Thorne, J.L., Bruno, W.J., 2001. Performance of a diver- work, occurred in the Plio-Pleistocene boundary gence time estimation method under a probabilistic model of rate t § evolution. Mol. Biol. Evol. 18, 352–361. 1.74 0.59 Mya (Fig. 2). The divergence of Octodonto- Lessa, E.P., Cook, J.A., 1998. The molecular phylogenetics of tuco- mys gliroides and Octodon+Spalacopus+Aconaemys tucos (genus Ctenomys, Rodentia: Octodontidae) suggests an early genera would have occurred during the late Miocene, burst of speciation. Mol. Phylogenet. Evol. 9, 88–99. around 6.07§1.34 Mya (2). This value is in agreement Rowe, D.L., Honeycutt, R.L., 2002. Phylogenetic relationships, ecologi- with the estimation based on DNA hybridization cal correlates, and molecular evolution within the cavioidea (Mam- malia, Rodentia). Mol. Biol. Evol. 19, 263–277. (Gallardo and Kirsch, 2001), but is older than the esti- Sanderson, M.J., 1997. A nonparametric approach to estimating diver- mation of Honeycutt et al., 2003) (Table 2). Divergence gence times in the absence of rate constancy. Mol. Biol. Evol. 14, between the genera Octodon, Spalacopus, and 1218–1232. J.C. Opazo / Molecular Phylogenetics and Evolution 37 (2005) 932–937 937

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