Sciurid phylogeny and the evolution of African ground squirrels

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Sciurid phylogenyand the evolution ofAfrican
ground squirrels

• Matthew D. HerronUniversity of Central Florida
• Department of Biology

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Seminar outline

• Part 1 Sciurid phylogeny
• Higher level evolutionary relationships
• Relationships within the tribe Marmotini
• Taxonomy vs. phylogeny
• Part 2 Evolution of African ground squirrels
• Evolutionary relationships within the tribe
  Xerini
• Phylogeography of Xerus inauris

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Family Sciuridae(Mammalia Rodentia)

• Tree squirrels Sciurus, Microsciurus,
  Tamiasciurus
• Flying squirrels Glaucomys, Pteromys
• Chipmunks Tamias
• Ground squirrels Spermophilus, Ammospermophilus
• Prairie dogs Cynomys
• Marmots - Marmota
• African ground squirrels Xerus

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Family Sciuridae

• Widespread all continents except Australia
  Antarctica
• Conspicuous large, mostly diurnal
• Phylogeny poorly known

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Family Sciuridae

• Wide range of ecological, behavioral and life
  history traits
• Terrestrial, fossorial, arboreal
• Habitats from tundra to desert
• Solitary to highly social
• Ideal subjects for studies of character evolution
• Several comparative studies of behavioral and
  life history traits limited by
• Phylogenies based on limited taxonomic sampling
• Taxonomy, rather than phylogeny, used as a basis
  for comparison

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Objectives

• To develop hypotheses of the evolutionary history
  of the family Sciuridae
• Reconstruct the evolutionary history (phylogeny)
  of the group
• Compare current taxonomy with proposed phylogeny
• A robust phylogeny with extensive taxon sampling
  will facilitate analyses of character evolution

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Strategy

• Sequenced the mitochondrial cytochrome b gene
• 1140 base pairs
• Widely used for phylogenetic analyses
• Large number of sequences available

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Methods

• Extract DNA from hair and tissue samples using
  phenol/chloroform
• PCR and sequence mt cyt-b gene (1140 bp)

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Taxon sampling

• Available sequences were downloaded from GenBank
• Two novel sequences (Xerus inauris, X. rutilus)
  were generated for this study
• Taxon sampling
• 114 species in 21 genera
• Multiple individuals included when available
• Multiple named subspecies included when available
• Total of 169 OTUs

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Analyses

• Sequences were aligned in GeneDoc
• Maximum parsimony analyses in PAUP
• Smallest number of mutational steps
• Nodal support assessed with 300 bootstrap
  pseudoreplicates (BS)
• Bayesian analyses in MrBayes
• Model-based approach
• Nodal support assessed with Bayesian posterior
  probabilities (BPP)

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Results ofphylogenetic analyses
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Outgroups
99
Sciurillus
Xerini

93
Callosciurus

Tamiasciurus
98
Sciurus
60


Flying squirrels
Results Bayesian phylogram for the Sciuridae
70
99


Tamiini
99
76
100
100
Marmotini
10 Changes
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Differences among studies
Sciurillus
Sciurillus
Sciurillus
Sciurini/ Pteromyinae
Sciurini/ Pteromyinae
Xerini
Xerini
Callosciurini
Xerini
Sciurini/ Pteromyinae
Callosciurini
Callosciurini
Mercer Roth 2003 2659 nuclear mt bp 54
species in 50 genera
Steppan, et al. in press 4500 nuclear bp 34
species in 24 genera
Herron, et al. in press 1140 mt bp 114 species
in 21 genera
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Outgroups
99
Sciurillus
Xerini

93
Callosciurus

Tamiasciurus
98
Sciurus
60


Flying squirrels
Results Bayesian phylogram for the Sciuridae
70
99


Tamiini
99
76
100
100
Marmotini
10 Changes
16
100
Tamiasciurus
100
100
78
Sciurus
100
92
Microsciurus
Pteromys
99
Petaurista

Belomys
Hylopetes
Petinomys
Glaucomys
10 Changes
Tree squirrels flying squirrels
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Eutamias
72
Tamias

100
100
Neotamias
Chipmunks
10 Changes
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Summary

• Flying squirrels are monophyletic, sister to tree
  squirrels
• Sciurillus phylogenetic position does not agree
  with taxonomy
• Sciurus is paraphyletic with respect to
  Microsciurus

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Outgroups
99
Sciurillus
Xerini

93
Callosciurus

Tamiasciurus
98
Sciurus
60


Flying squirrels
Results Bayesian phylogram for the Sciuridae
70
99


Tamiini
99
76
100
100
Marmotini
10 Changes
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Tribe Marmotini
Spermophilus
Marmota
Ammospermophilus
Cynomys
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Tribe Marmotini

• gt60 species in 4 genera
• Holarctic distribution
• Europe east of the Alps
• Asia
• North America

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90
Ammospermophilus
85
100
Cynomys
100
100
100
Marmota
10 Changes
23
Ground Squirrels
100
Poliocitellus
100
100
Xerospermophilus
87
100
Callospermophilus
88
10 Changes
24
100
60
Otospermophilus
Ground Squirrels
99
52
Ammospermophilus
100
Otospermophilus
100
92
88
Callospermophilus
10 Changes
25
Ground Squirrels
New World
99
90
Spermophilus
S. undulatus
100
92
Old World
Spermophilus
10 Changes
26
Ground Squirrels
100
Ictidomys
98
100
54
94
57
100
Ictidomys
100
10 Changes
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Summary - Marmotini

• Cynomys, Marmota, Ammospermophilus monophyletic
• Spermophilus paraphyletic w/ respect to
• Ammospermophilus
• Cynomys
• Marmota
• Diphyletic Spermophilus subgenera
• Spermophilus
• Ictidomys
• Otospermophilus

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Conclusions Part 1

• Sciurid taxonomy has problems at all levels
• Subfamily designations are not phylogenetically
  informative
• Sciurillus does not belong in tribe Sciurini
• Sciurus is paraphyletic with respect to
  Microsciurus
• Spermophilus is polyphyletic
• Genus, subgenera and even some species have
  multiple origins
• Elevating subgenera will not resolve

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Xerini - differences among studies
Sciurillus
Sciurillus
Sciurillus
Sciurini/ Pteromyinae
Sciurini/ Pteromyinae
Xerini
Xerini
Callosciurini
Xerini
Sciurini/ Pteromyinae
Callosciurini
Callosciurini
Mercer Roth 2003
Steppan, et al. in press
Herron, et al. in press
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Atlantoxerus
Spermophilopsis
X. erythropus
X. rutilus
X. princeps
X. inauris
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Xerine phylogeny background
Spermophilopsis

• Intergeneric relationships based on DNA sequence
  data

Atlantoxerus
Xerus
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Xerine phylogeny background
X. rutilus

• Xerus relationships based on skull and dental
  morphology

X. erythropus
X. inauris
X. princeps
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Are X. inauris X. princeps specifically
distinct?
Xerus inauris
Xerus princeps
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Are X. inauris X. princeps distinct species?

• Behavioral differences
• X. inauris is highly social
• Both male and female social groups
• X. princeps is essentially asocial

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Objectives

• Infer phylogenetic hypotheses for the four
  recognized species of Xerus
• Estimate historical biogeographic patterns
  leading to current distributions of Xerus species
• Establish roles of gene flow and climate change
  in the phylogeographic history of X. inauris
• Assess the validity of the specific distinction
  between X. inauris and X. princeps

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Methods

• Extract DNA from hair and tissue samples using
  phenol/chloroform
• PCR and sequence mt cyt-b gene (1140 bp)

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Taxon sampling

• cyt b sequences obtained for
• 3 X. erythropus
• 66 X. inauris
• 9 X. princeps
• 2 X. rutilus
• Spermophilopsis leptodactylus used as outgroup in
  all phylogenetic analyses

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Analyses

• Sequences were aligned in GeneDoc
• Bayesian analysis in MrBayes
• Nodal support assessed with Bayesian posterior
  probabilities
• Maximum parsimony analysis in PAUP
• Nodal support assessed with 500 bootstrap
  pseudoreplicates

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Spermophilopsis leptodactylus
100
Xerus erythropus
100
90
X. rutilus
100
100
75
X. princeps
100
59
100
100
99
100
Results Bayesian phylogram of Xerus
X. inauris
5 changes
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Biogeography of Africa

• Well-known pattern of plant disjunctions between
  the Horn of Africa and the Cape of Good Hope
• Hypothesized arid corridor from eastern to
  southern Africa
• Southern Africa climate change in the Pliocene
  and Pleistocene
• Several wet-dry cycles
• Temperature change due to glaciation

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X. rutilus
X. erythropus
X. princeps
X. inauris
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Spermophilopsis leptodactylus
Xerus erythropus
Xerus rutilus
X. princeps
I
Genetic structure of X. inauris X. princeps
II
X. inauris
I
III
III
II
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Methods nested clade analysis

• Haplotype network reconstructed with parsimony
  criterion in TCS
• Similar haplotypes hierarchically nested into
  progressively older and larger clades
• Clades tested for associations with geographic
  distance in GeoDis
• Used to infer historical processes leading to
  present distributions

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Xerus inauris nested cladogram
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Results of NCA

• Restricted gene flow with isolation by distance
  (IBD) inferred for older clades
• IBD for a maternally inherited marker is
  congruent with X. inauris social system (female
  philopatry)
• Suggests xeric conditions were widespread early
  in the species history

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Results of NCA

• Habitat fragmentation inferred for one more
  recent clade
• Suggests interruption of continuous arid
  conditions
• Congruent with wet-dry cycles in the Late
  Pliocene and Pleistocene
• Southern Africa is low in elevation, so small
  changes in precipitation would cause large
  changes in vegetation

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Biogeographic summary

• Xeric conditions widespread in southern Africa
  early in X. inauris evolution
• Xeric conditions interrupted by Plio-Pleistocene
  wet-dry cycles
• Arid corridor from Horn of Africa to Cape of
  Good Hope lasted at least until the Early
  Pleistocene

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Species status

• X. inauris, X. princeps are well supported,
  reciprocally monophyletic clades
• Highest sequence divergence within taxa (4) is
  less than lowest divergence between taxa (6)
• Sympatric ranges, overlapping habitats
• Suggests that reproductive isolation results from
  factors other than geography

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Other differences betweenX. inauris and X.
princeps

• Single heterochromatic difference in one
  autosomal chromosome pair
• Differences in thermoregulation and urine and
  fecal content
• Minor differences in skull morphology

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Summary

• Higher-level taxonomy of squirrels needs revision
• Spermophilus is polyphyletic
• Sciurus paraphyletic with respect to Microsciurus
• Sciurillus basal to remaining sciurids
• Flying squirrels monophyletic, sister to tree
  squirrels

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Acknowledgments

• Dr. Chris Parkinson
• Dr. Jane Waterman
• Dr. Franklin Snelson
• Dr. James Roth
• Todd Castoe
• Dr. John Fauth
• Dr. Walter Sotero
• Beryl Wilson
• Jo Newman
• Dr. Tatsuo Oshida
• Dr. Eileen Lacey
• Dr. Mary Denver
• Sue McLaren