1. Nick Milne & Cyril Grueter
Investigating the relationship between sexual dimorphism and mating system
in Macropodidae
Hazel Richards
Nick Milne & Cyril Grueter
School of Anatomy, Physiology and Human Biology, The University of Western Australia

2. Sexual dimorphism
Differences between males and females of a species (colour, displays, weaponry, size)
Size dimorphism commonly expressed as male : female ratio
Images: Wikimedia Commons, Flickr Commons

3. Sexual dimorphism
Differences between males and females of a species (colour, displays, weaponry, size)
Size dimorphism commonly expressed as male : female ratio
Thoroughly examined in primates (body size, colour, canines)
Images: Wikimedia Commons, Flickr Commons

4. Sexual dimorphism
Differences between males and females of a species (colour, displays, weaponry, size)
Size dimorphism commonly expressed as male : female ratio
Thoroughly examined in primates (body size, colour, canines)
Dimorphism in body size & weaponry arise from sexual selection via intermale competition for mates
Dimorphism corresponds with mating systems in primates
Images: Wikimedia Commons, Flickr Commons

5. Sexual dimorphism
Differences between males and females of a species (colour, displays, weaponry, size)
Size dimorphism commonly expressed as male : female ratio
Thoroughly examined in primates (body size, colour, canines)
Dimorphism in body size & weaponry arise from sexual selection via intermale competition for mates
Dimorphism corresponds with mating systems in macropodids?
Images: Wikimedia Commons, Flickr Commons

6. Macropodids Family Macropodidae “big foot” Kangaroos & wallabies
Hare wallabies
Rock wallabies
Nailtail wallabies
Pademelons
Quokka
Tree kangaroos

7. Macropodids Family Macropodidae “big foot” Not tree kangaroos
Kangaroos & wallabies
Hare wallabies
Rock wallabies
Nailtail wallabies
Pademelons
Quokka
Tree kangaroos

8. Macropodids Family Macropodidae “big foot” Not tree kangaroos
Differing levels of sexual dimorphism
Kangaroos & wallabies
Hare wallabies
Rock wallabies
Nailtail wallabies
Pademelons
Quokka
Tree kangaroos

9. Macropodids Family Macropodidae “big foot” Not tree kangaroos
Differing levels of sexual dimorphism
Body size

10. Macropodids Family Macropodidae “big foot” Not tree kangaroos
Differing levels of sexual dimorphism
Body size

11. Macropodids Family Macropodidae “big foot” Not tree kangaroos
Differing levels of sexual dimorphism
Body size
Fore limb
Top species shows moderate dimorphism in body size (visible in head length difference)
Bottom species shows similar body size, but large dimorphism in upper limb bones (humerus and scapula)

12. Macropodids Family Macropodidae “big foot” Not tree kangaroos
Differing levels of sexual dimorphism
Body size
Fore limb
Top species shows moderate dimorphism in body size (visible in head length difference)
Bottom species shows similar body size, but large dimorphism in upper limb bones (humerus and scapula)

13. Macropodids Family Macropodidae “big foot” Not tree kangaroos
Differing levels of sexual dimorphism
Body size
Fore limb
Range of mating systems described in the literature (fitted to model described by Clutton-Brock 1989)

14. Mating systems Monogamous Hare wallabies Some rock wallabies
Monogamous: Males and female solitary. Males territorial, but with the very low population density results in very low male competition levels.
Hare wallabies
Some rock wallabies
all < 10kg

15. Mating systems Monogamous Polygynous Hare wallabies
Polygynous: Females are found in small groups that share a small home range, with a single male defending this range and the females within it. There is a higher population density and consequently males come across one another more often than in the monogamous system, creating higher male competition.
Hare wallabies
Some rock wallabies
all < 10kg
Most rock wallabies
Quokka
all < 10kg

16. Mating systems 1 Monogamous Polygynous Promiscuous 2 3
Promiscuous: Females are gregarious and unpredictably distributed in the environment. Males are non-territorial, but are arranged into a size-based dominance hierarchy that determines which male has exclusive access to females. This results in a high reproductive skew, with a single male monopolising matings, and therefore male competition for this top spot in the hierarchy is very strong. 2 3
Kangaroos & wallabies
Pademelons
Nailtail wallabies
4 – 40kg
Hare wallabies
Some rock wallabies
all < 10kg
Most rock wallabies
Quokka
all < 10kg

17. Hypotheses Species under 10kg: Sexual dimorphism cranial length
limb proportions
Monogamy
Polygyny
Promiscuity
< 10kg
Monogamy
Polygyny
Promiscuity
< 10kg

18. Sample Six museum collections (WA, QLD, NSW, ACT, VIC, SA)
32 macropodid species from 7 genera
Six measurements:
1600 crania
390 humeri
360 radii
410 femora
380 tibiae
320 metatarsals

19. Limb proportions
Image: Hume at al. (1989)

20. Limb proportions Brachial index (BI) Radius / humerus
Image: Hume at al. (1989)

21. Limb proportions Brachial index (BI) Intermembral index (IMI)
Radius / humerus
Intermembral index (IMI)
Fore limb / hind limb
Brachial index measures the internal proportions of the upper limb, and indicates adaptations for speed or power in the forelimb
Intermembral index measures the proportion of the total upper to total lower limb, and is normally used to characterise locomotor patterns in primates (eg. High IMI for brachiators, equal in quadrupeds, low for bipeds). All macropodids are bipedal hoppers so have a low IMI, but I am using it to detect any relative size increase in the forelimb
Image: Hume at al. (1989)

22. Limb proportions Brachial index (BI) Intermembral index (IMI)
Radius / humerus
Intermembral index (IMI)
Fore limb / hind limb
Tibioradial index (TRI)
Radius / tibia
Image: Hume at al. (1989)

23. Limb proportions Brachial index (BI) Intermembral index (IMI)
Radius / humerus
Intermembral index (IMI)
Fore limb / hind limb
Tibioradial index (TRI)
Radius / tibia
Femorohumeral index (FHI)
Humerus / femur
TRI and FHI are subsets of IMI, used to tease apart any differences seen
Image: Hume at al. (1989)

24. Limb proportions Brachial index (BI) Intermembral index (IMI)
Radius / humerus
Intermembral index (IMI)
Fore limb / hind limb
Tibioradial index (TRI)
Radius / tibia
Femorohumeral index (FHI)
Humerus / femur
Metatarso-radial ratio (MRR)
Radius / metatarsal
MRR is not a functional index, but is adapted from some published work on macropodids where it was used to characterise exaggeration of the forelimb
Image: Hume at al. (1989)

25. Limb proportions Brachial index (BI) Intermembral index (IMI)
Radius / humerus
Intermembral index (IMI)
Fore limb / hind limb
Means of male and female per species, male : female ratios show dimorphism
Tibioradial index (TRI)
Radius / tibia
Femorohumeral index (FHI)
Humerus / femur
Metatarso-radial ratio (MRR)
Radius / metatarsal
Image: Hume at al. (1989)

26. Adjusting for age posterior Indeterminate growth (older = larger)
Macropod molars erupt and move forward with age
Molar index (MI) provides relative age within a species
condense
anterior
Figure: Kirkpatrick (1964)

27. Adjusting for age posterior Indeterminate growth (older = larger)
Macropod molars erupt and move forward with age
Molar index (MI) provides relative age within a species
All species studied reach sexual maturity by MI = 2
Linear regression to adjust each sexes crania to MI = 2.5, took male and female means
anterior
Figure: Kirkpatrick (1964)

28. Adjusting for age posterior Indeterminate growth (older = larger)
Macropod molars erupt and move forward with age
Molar index (MI) provides relative age within a species
All species studied reach sexual maturity by MI = 2
Linear regression to adjust each sexes crania to MI = 2.5, took male and female means
Means significantly correlated with body mass (rs = .94)
Male : female ratio cranial length
Limb indices did not change with age
anterior
Figure: Kirkpatrick (1964)

29. Hypothesis 1 – Mating system and size dimorphism
Sexual dimorphism
cranial length
Monogamous
Polygynous
Promiscuous
< 10kg

30. Results – Mating system and size dimorphism
Monogamous
Promiscuous
< 10kg
Polygynous
Ratio M : F cranial length
Dimorphism in cranial length increased significantly across mating systems (Jonckheere’s trend test p = 0.01)
Hypothesis supported

31. Sexual dimorphism – Limb proportions
Males generally have larger forelimbs than females
Used for display and fighting, intensity and frequency differs between species
Jarman, PJ 1989, ‘Sexual dimorphism in Macropodoidea’, in Kangaroos, Wallabies & Rat-kangaroos

32. Sexual dimorphism – Limb proportions
Males generally have larger forelimbs than females
Used for display and fighting, intensity and frequency differs between species
Jarman (1989) compared forearm with foot to show dimorphism (MRR)
Jarman, PJ 1989, ‘Sexual dimorphism in Macropodoidea’, in Kangaroos, Wallabies & Rat-kangaroos

33. Sexual dimorphism – Limb proportions
Males generally have larger forelimbs than females
Used for display and fighting, intensity and frequency differs between species
Jarman (1989) compared forearm with foot to show dimorphism (MRR)
Mating system - Hypothesis 2
Jarman, PJ 1989, ‘Sexual dimorphism in Macropodoidea’, in Kangaroos, Wallabies & Rat-kangaroos

34. Hypothesis 2 – Mating system and limb dimorphism
Sexual dimorphism
limb proportions
Monogamous
Polygynous
Promiscuous
< 10kg

35. Results – Mating system and limb dimorphism
Monogamous
Promiscuous
< 10kg
Polygynous
Ratio M : F Metatarso-radial ratio
Ratio M : F Tibioradial index
Monogamous
Promiscuous
< 10kg
Polygynous
TRI and MRR increased significantly across mating systems
(Jonckheere’s trend test, p = 0.02, p = 0.04)
Weak trend also seen in IMI (p = 0.09)
Not significant in BI and FHI  male radius getting longer relative to hind limb

36. Discussion – Mating system and sexual dimorphism
Larger body size and longer forelimb in more promiscuous males – why?

37. Discussion – Mating system and sexual dimorphism
Larger body size and longer forelimb in more promiscuous males – why?
Monogamous
Hare wallabies
Rock wallabies
Polygynous
Quokka
Promiscuous
Small wallabies
Pademelons
Male fighting
Rare
Infrequent
Frequent
Male competition
Low
Intermediate
High

38. Discussion – Mating system and sexual dimorphism
Larger body size and longer forelimb in more promiscuous males – why?
Monogamous
Hare wallabies
Rock wallabies
Polygynous
Quokka
Promiscuous
Small wallabies
Pademelons
Male fighting
Rare
Infrequent
Frequent
Male competition
Low
Intermediate
High
Higher frequency of male fighting  increased male competition 
stronger sexual selection on traits that win fights

39. Discussion – Mating system and sexual dimorphism
Larger body size and longer forelimb in more promiscuous males – why?
Monogamous
Hare wallabies
Rock wallabies
Polygynous
Quokka
Promiscuous
Small wallabies
Pademelons
Male fighting
Rare
Infrequent
Frequent
Male competition
Low
Intermediate
High
Higher frequency of male fighting  increased male competition 
stronger sexual selection on traits that win fights
Larger body size – defend territory, ascend dominance hierarchy
Longer forelimb – better reach during grapple, quicker movements?

40. Conclusions
Increased dimorphism in cranial length in more promiscuous species
Supports patterns seen in primates and other mammals
Image: Wikimedia Commons

41. Conclusions
Increased dimorphism in cranial length in more promiscuous species
Supports patterns seen in primates and other mammals
Increased dimorphism in relative forelimb length in more promiscuous species
Body size result fits well with understanding of dimorphism in mammals
Limb difference is an interesting result in evolutionary context – normally dimorphism occurs in extraneous male anatomy used for little else (horns, canine teeth in herbivorous primates etc.)
Macropodid upper limb used for grooming, foraging etc.
Image: Wikimedia Commons

42. Conclusions
Increased dimorphism in cranial length in more promiscuous species
Supports patterns seen in primates and other mammals
Increased dimorphism in relative forelimb length in more promiscuous species
Unique that the limb is the sexually- selected weapon
Unlike horns, canines in other species
Used by both sexes
Body size result fits well with understanding of dimorphism in mammals
Limb difference is an interesting result in evolutionary context – normally dimorphism occurs in extraneous male anatomy used for little else (horns, canine teeth in herbivorous primates etc.)
Macropodid upper limb used for grooming, foraging etc.
Image: Wikimedia Commons

43. Future work Phylogenetic control Mixed discrete and continuous data
Image: Wikimedia Commons

44. Future work Phylogenetic control
Mixed discrete and continuous data
Characterise more aspects of bone morphology
Crania – Shape analysis (GM)
Limbs – Mid-shaft diameter (robustness), shape analysis (GM)
Image: Wikimedia Commons

45. Future work Phylogenetic control
Mixed discrete and continuous data
Characterise more aspects of bone morphology
Crania – Shape analysis (GM)
Limbs – Mid-shaft diameter (robustness), shape analysis (GM)
Mating system classification
Microsatellite paternity studies, testicular volume
Image: Wikimedia Commons

46. Future work Phylogenetic control
Mixed discrete and continuous data
Characterise more aspects of bone morphology
Crania – Shape analysis (GM)
Limbs – Mid-shaft diameter (robustness), shape analysis (GM)
Mating system classification
Microsatellite paternity studies, testicular volume
Database to target individual specimens or taxa for more specific measurements and hypothesis testing
Sexed macropodid specimens in 6 museum collections, including molar index
Image: Wikimedia Commons

47. Acknowledgements Nick Milne and Cyril Grueter
Collection managers – WA Museum, QLD Museum, Australian Museum, Australian National Wildlife Collection, Museum Victoria and SA Museum
Dr. Margaret Loman-Hall scholarship
Image: Wikimedia Commons