Mark S. Hafner

BASAL CLADES AND MOLECULAR SYSTEMATICS OF HETEROMYID RODENTS

Abstract The New World rodent family Heteromyidae shows a marvelous array of ecomorphological types, from bipedal, arid-adapted forms to scansorial, tropical-adapted forms. Although recent studies have resolved most of the phylogenetic relationships among heteromyids at the shallower taxonomic levels, fundamental questions at the deeper taxonomic levels remain unresolved. This study relies on DNA sequence information from 3 relatively slowly evolving mitochondrial genes, cytochrome c oxidase subunit I, 12S, and 16S, to examine basal patterns of phylogenesis in the Heteromyidae. Because slowly evolving mitochondrial genes evolve and coalesce more rapidly than most nuclear genes, they may be superior to nuclear genes for resolving short, basal branches. Our molecular data (2,381 base pairs for the 3-gene data set) affirm the monophyly of the family and resolve the major basal clades in the family. Alternative phylogenetic hypotheses of subfamilial relationships are examined statistically and the Perognathinae and Heteromyinae are found to represent sister clades relative to the Dipodomyinae. The 3 traditional subfamilial groupings are supported; the controversial placement of Microdipodops as a sister clade to Dipodomys in the Dipodomyinae is affirmed, Perognathus and Chaetodipus are distinct sister clades within the Perognathinae, and species of Liomys and Heteromys form the resolved clade Heteromyinae. However, Liomys is found to be paraphyletic relative to Heteromys and, given that this finding corroborates earlier studies, we present a formal taxonomy of Heteromys wherein we place Liomys in synonymy. Semiparametric and parametric methods are used to estimate divergence times from our molecular data and a chronogram of the Heteromyidae, calibrated by the oldest known fossils of Dipodomys and Perognathus, is presented. Our time estimates reveal subfamilial differentiation in the early Miocene (22.3–21.8 million years ago) and pose testable times of divergence for the basal heteromyid nodes. With the basal heteromyid clades resolved and cladogenic events positioned in a time framework, we review the major geological and paleoecological events of the Oligocene and Miocene associated with the early historical biogeography of the family.

DIFFERENCES IN RATE OF CYTOCHROME-b EVOLUTION AMONG SPECIES OF RODENTS

Abstract Although molecular evolution often appears to proceed in a clocklike fashion, examples to the contrary are increasing in number. Our study compares rate of cytochrome-b evolution in 21 rodent species, each of which belongs to a different genus. In these comparisons, substitutions at synonymous sites appear to be saturated, precluding inferences about rate of synonymous substitution. Rate of nonsynonymous substitution differs significantly among many of the rodents studied. However, the cause or causes of these differences in substitution rate remains in question. Differences in generation time, body size, or metabolic rate do not seem to be associated with rate of nonsynonymous substitution in these rodents. Effective population size remains a viable explanation of the observed rate heterogeneity. However, we suggest that a search for simple causes of differences in rate of molecular evolution may be difficult in light of numerous aspects of an organisms biology that may together influence evolutionary rates over space and time.

Tactile discriminatory ability and foraging strategies in Kangaroo rats and pocket mice (Rodentia: Heteromyidae)

SummaryA comparative study of seasonal food hoarding activity and tactile discriminatory ability in four species of heteromyid rodents (Dipodomys panamintinus, D. merriami, Perognathus longimembris, and P. formosus) was conducted in laboratory test arenas. Animals were tested individually to determine their treatment of seed (white millet) and seed mimics (glass beads and gravel) offered as food. In general, all animals showed low levels of millet hoarding activity during winter months with higher levels in fall and spring. Observations revealed that all species manipulated (with the forepaws) each potential food item prior to eating, pouching, or rejecting it. These tactile cues appear to surpass visual and olfactory cues as critical factors in distinguishing between food and food mimics. Pocket mice (Perognathus) showed high levels of tactile discriminatory ability which may serve as the mechanism by which they achieve high foraging efficiency in nature when “filter-feeding” for widely dispersed seed resources. Kangaroo rats (Dipodomys), on the other hand, are less adept at distinguishing between food and very similar non-food items. The fact that, in nature, kangaroo rats depend heavily on clumped food resources may obviate the need for highly efficient tactile discriminatory abilities.

HYBRID ZONES IN THOMOMYS BOTTAE POCKET GOPHERS: GENETIC, PHENETIC, AND ECOLOGIC CONCORDANCE PATTERNS

In a recent summary of geographic variability of both chromosomal and genic systems in Thomomys bottae pocket gophers, Patton and Yang (1977) presented data depicting extensive degrees of interpopulation genetic divergence. In several instances, adjacent or near adjacent pairs of populations were seen to differ by lOIS fixed chromosomal rearrangements and to share less than 80% in overall allelic similarity in structural genes as measured by starch gel electrophoresis. Despite the enormity of observed interpopulation divergence (in many cases greater than that found between species of other mammals), available data suggested that these geographic segments retained the ability to interbreed. Evidence for this conclusion came from studies by other workers suggesting intergradation between several of the differentiated units based on the morphological intermediacy of some specimens. In no study, however, had the gross morphological indications of intergradation been fully supported by genetic analyses. The purpose of the present report is to provide a concomitant comparison of intergradation from a genetic, morphologic, and ecologic perspective between two of the most strongly differentiated, geographically adjacent units of T. bottae that were recognized by Patton and Yang (1977). Pocket gophers of the conifer forest zones of the White and Sacramento mountains of south central New Mexico, described as T. b . ruidosae by Hall (1932), are characterized by moderate size, dark coloration, and a karyotype composed of nearly all biarmed autosomes (2n = 76). This form meets T. b. actuosus Kelson Revised December 16, 1978

Host specificity of chewing lice on pocket gophers : A potential mechanism for cospeciation

Pocket gophers (Rodentia: Geomyidae) and their ectoparasitic chewing lice (Phthiraptera Trichodectidae) have congruent phylogenies and show evidence of cospeciation. We examined a potential mechanism that could generate the observed pattern of cospeciation by testing the ability of lice to survive and reproduce on hosts other than their own. Our tests were conducted at the subspecific, specific, and generic levels relative to the natural host. Although lice established successful colonies at each level, colonization of new hosts diminished with increasing phylogenetic distance from the natural host of each louse. We suggest that the pattern of cospeciation results primarily from lack of opportunity for lice to colonize new hosts. However, in rare cases where lice disperse to new hosts, survival may be difficult on hosts that are not closely related to the natural host, which would reinforce the pattern of cospeciation.

Macrogeographic Patterns of Genetic Differentiation in the Pocket Gopher Thomomys Umbrinus

Electromorphic and chromosomal variation is analyzed in 26 populations of Tho- momys umbrinus sampled from throughout the range of the species. Interpopulation levels of genic differentiation are extreme, generally exceeding values measured between conspecific populations of most animals or plants. Two principal groups of T. umbrinus are recognized based on chromosomal evidence, one with 2n = 76 chromosomes and the other with 2n = 78. Further, the 2n = 78 group (but not the 2n = 76 group) is bisected into geographic subgroups with respect to chromosome morphology and heterochromatin position. The kind and degree of chromosomal differentiation observed suggests that the three groups may be reproductively incompatible. Allozymic evidence corroborates the above groupings, and an analysis of patterns of allele sharing suggests the absence of gene flow among the groups. A cladistic analysis of electro- morphic data indicates that the two 2n = 78 groups may be independently derived from the 2n = 76 lineage. The combined evidence supports the hypothesis that T. umbrinus is actually a composite of at least three biological species and confirms the observation that speciation in the genus Thomomys is unrelated to the level of genic differentiation between populations. (Evolu- tionary genetics; geographic variation; evolutionary concordance; pocket gophers; cladistic anal- ysis; paraphyly; speciation.)

Codivergence in heteromyid rodents (Rodentia: heteromyidae) and their sucking lice of the genus Fahrenholzia (Phthiraptera: anoplura).

Although most studies of codivergence rely primarily on topological comparisons of host and parasite phylogenies, temporal assessments are necessary to determine if divergence events in host and parasite trees occurred contemporaneously. A combination of cophylogenetic analyses and comparisons of branch lengths are used in this study to understand the host-parasite association between heteromyid rodents (Rodentia: Heteromyidae) and their sucking lice of the genus Fahrenholzia (Phthiraptera: Anoplura). Cophylogenetic comparisons based on nucleotide substitutions in the mitochondrial COI gene reveal a significant, but not perfect, pattern of cophylogeny between heteromyids and their sucking lice. Regression analyses show a significant functional relationship between the lengths of analogous branches in the host and parasite trees, indicating that divergence events in hosts and parasites were approximately contemporaneous. Thus, the topological similarity observed between heteromyids and their lice is the result of codivergence. These analyses also show that the COI gene in lice is evolving two to three times faster than the same gene in their hosts (similar to the results of studies of other lice and their vertebrate hosts) and that divergence events in lice occurred shortly after host divergence. We recommend that future studies of codivergence include temporal comparisons and, when possible, use the same molecular marker(s) in hosts and parasites to achieve the greatest insight into the history of the host-parasite relationship.

On transition bias in mitochondrial genes of pocket gophers

The relative contribution of mutation and purifying selection to transition bias has not been quantitatively assessed in mitochondrial protein genes. The observed transition/transversion (s/v) ratio is (μsPs)/(μvPv), where μs and μv denote mutation rate of transitions and transversions, respectively, andPs andPv denote fixation probabilities of transitions and transversions, respectively. Because selection against synonymous transitions can be assumed to be roughly equal to that against synonymous transversions,Ps/Pv ≈ 1 at fourfold degenerate sites, so that thes/v ratio at fourfold degenerate sites is approximately μs/μv, which is a measure of mutational contribution to transition bias. Similarly, thes/v ratio at nondegenerate sites is also an estimate of μs/μv if we assume that selection against nonsynonymous transitions is roughly equal to that against nonsynonymous transversions. In two mitochondrial genes, cytochrome oxidase subunit I (COI) and cytochromeb (cyt-b) in pocket gophers, thes/v ratio is about two at nondegenerate and fourfold degenerate sites for both the COI and the cyt-b genes. This implies that mutation contribution to transition bias is relatively small. In contrast, thes/v ratio is much greater at twofold degenerate sites, being 48 for COI and 40 for cyt-b. Given that the μs/μv ratio is about 2, thePs/Pv ratio at twofold degenerate sites must be on the order of 20 or greater. This suggests a great effect of purifying selection on transition bias in mitochondrial protein genes because transitions are synonymous and transversions are nonsynonymous at twofold degenerate sites in mammalian mitochondrial genes. We also found that nonsynonymous mutations at twofold degenerate sites are more neutral than nonsynonymous mutations at nondegenerate sites, and that the COI gene is subject to stronger purifying selection than is the cyt-b gene. A model is presented to integrate the effect of purifying selection, codon bias, DNA repair and GC content ons/v ratio of protein-coding genes.

DNA Data Support a Rapid Radiation of Pocket Gopher Genera (Rodentia: Geomyidae)

In this study, we address the question of phylogenetic relationships in the Geomyidae, focusing primarily on intergeneric relationships within the tribe Geomyini. Our study makes use of DNA sequences from two mitochondrial and two nuclear genes, and we use model-based methods of phylogenetic analysis to infer relationships and determine the level of support for each proposed relationship. Relationships among geomyine pocket gopher genera remain only partially resolved despite a number of earlier attempts to reconstruct their phylogenetic history and despite the newly generated sequence data analyzed in this study. This lack of resolution does not appear to result from insufficient or inappropriate DNA data, nor is it caused by inadequate sampling of taxa. Rather, molecular data and fossil data together lead to the conclusion that diversification within the Geomyini likely occurred during a geologically brief period in the Blancan. Rapid climate change during the Blancan, the origin of patchily distributed grasslands, and the evolution of hypsodonty may have triggered the rapid diversification that eventually produced the five extant genera of the Geomyini.

Cospeciation of Pocket Gophers (Geomys) and their Chewing Lice (Geomydoecus)

Comparison of independently derived phylogenies for pocket gophers ( Geomys ) and their chewing lice ( Geomydoecus ) from Texas and Louisiana indicates a history of widespread cospeciation in this host-parasite assemblage. Inference of cospeciation is supported by statistical comparison of genetic-distance matrices for gophers and lice based on allozyme data. Although similar, host and parasite phylogenies are not identical; inconsistencies likely result from host-switching by the parasites, retention of ancestral taxa of parasites on recently evolved hosts, or poorly delineated taxonomic boundaries. The current disjunct distribution of Geomydoecus ewingi suggests that this chewing louse once parasitized the common ancestor of Geomys breviceps and G. attwateri . Combined protein and morphologic evidence suggests that the population of Geomydoecus ewingi hosted by G. breviceps breviceps in northeastern Louisiana may be a cryptic species of louse.