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Sciurid phylogeny and the evolution of African ground squirrels Matthew D. Herron University of Central Florida Department of Biology Seminar outline Part 1: Sciurid phylogeny Higher level evolutionary relationships Relationships within the tribe Marmotini Taxonomy vs. phylogeny

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sciurid phylogeny and the evolution of african ground squirrels

Sciurid phylogenyand the evolution ofAfrican ground squirrels

Matthew D. HerronUniversity of Central Florida

Department of Biology

seminar outline
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
slide3

Sciurus

carolinensis

Sciurus

niger

Rocky

Glaucomys volans

family sciuridae mammalia rodentia
Family Sciuridae(Mammalia: Rodentia)
  • Tree squirrels – Sciurus, Microsciurus, Tamiasciurus
  • Flying squirrels – Glaucomys, Pteromys
  • Chipmunks – Tamias
  • Groundsquirrels – Spermophilus, Ammospermophilus
  • Prairie dogs – Cynomys
  • Marmots - Marmota
  • African ground squirrels – Xerus
family sciuridae
Family Sciuridae
  • Widespread – all continents except Australia & Antarctica
  • Conspicuous – large, mostly diurnal
  • Phylogeny poorly known
family sciuridae6
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
objectives
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
strategy
Strategy
  • Sequenced the mitochondrial cytochrome b gene
    • 1140 base pairs
    • Widely used for phylogenetic analyses
    • Large number of sequences available
methods
Methods
  • Extract DNA from hair and tissue samples using phenol/chloroform
  • PCR and sequence mt cyt-b gene(1140 bp)
taxon sampling
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
analyses
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)
slide13

BPP

BS (* = <50%)

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

differences among studies
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

slide15

BPP

BS (* = <50%)

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

slide16

BPP

BS (* = <50%)

100

Tamiasciurus

100

100

78

Sciurus

100

92

Microsciurus

Pteromys

99

Petaurista

*

Belomys

Hylopetes

Petinomys

Glaucomys

10 Changes

Tree squirrels & flying squirrels

slide17

BPP

BS (* = <50%)

Eutamias

72

Tamias

*

100

100

Neotamias

Chipmunks

10 Changes

summary
Summary
  • Flying squirrels are monophyletic, sister to tree squirrels
  • Sciurillus phylogenetic position does not agree with taxonomy
  • Sciurus is paraphyletic with respect to Microsciurus
slide19

BPP

BS (* = <50%)

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

tribe marmotini
Tribe Marmotini

Spermophilus

Marmota

Ammospermophilus

Cynomys

tribe marmotini21
Tribe Marmotini
  • >60 species in 4 genera
  • Holarctic distribution:
    • Europe east of the Alps
    • Asia
    • North America
slide22

BPP

BS

90

Ammospermophilus

85

100

Cynomys

100

100

100

Marmota

10 Changes

slide23

BPP

BS

Ground Squirrels

100

Poliocitellus

100

100

Xerospermophilus

87

100

Callospermophilus

88

10 Changes

slide24

100

BPP

BS

60

Otospermophilus

Ground Squirrels

99

Ammospermophilus

52

100

Otospermophilus

100

92

88

Callospermophilus

10 Changes

slide25

BPP

BS

Ground Squirrels

New World

99

90

Spermophilus

+ S. undulatus

100

92

Old World

Spermophilus

10 Changes

slide26

BPP

BS (* = <50%)

Ground Squirrels

100

Ictidomys

98

100

54

94

57

100

Ictidomys

100

10 Changes

summary marmotini
Summary - Marmotini
  • Cynomys, Marmota, Ammospermophilus monophyletic
  • Spermophilus paraphyletic w/ respect to
    • Ammospermophilus
    • Cynomys
    • Marmota
  • Diphyletic Spermophilus subgenera:
    • Spermophilus
    • Ictidomys
    • Otospermophilus
conclusions part 1
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
xerini differences among studies
Xerini - differences among studies

Sciurillus

Sciurillus

Sciurillus

Sciurini/

Pteromyinae

Sciurini/

Pteromyinae

Xerini

Xerini

Callosciurini

Xerini

Sciurini/

Pteromyinae

Callosciurini

Callosciurini

Mercer & Roth 2003

Herron, et al.

in press

Steppan, et al.

in press

slide30

Atlantoxerus

Spermophilopsis

X. erythropus

X. rutilus

X. princeps

X. inauris

xerine phylogeny background
Xerine phylogeny – background

Spermophilopsis

  • Intergeneric relationships based on DNA sequence data

Atlantoxerus

Xerus

xerine phylogeny background32
Xerine phylogeny – background

X. rutilus

  • Xerus relationships based on skull and dental morphology

X. erythropus

X. inauris

X. princeps

are x inauris x princeps distinct species
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
objectives35
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
methods36
Methods
  • Extract DNA from hair and tissue samples using phenol/chloroform
  • PCR and sequence mt cyt-b gene(1140 bp)
taxon sampling37
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
analyses38
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
slide39

BPP

BS

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

biogeography of africa
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
slide41

X. rutilus

X. erythropus

X. princeps

X. inauris

slide42

Spermophilopsis leptodactylus

Xerus erythropus

Xerus rutilus

X. princeps

I

Genetic structure of

X. inauris & X. princeps

II

X. inauris

I

III

III

II

methods nested clade analysis
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
slide44

Xerus inauris

nested cladogram

results of nca
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
results of nca46
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
biogeographic summary
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
species status
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
other differences between x inauris and x princeps
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
summary50
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
acknowledgments
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