The 3 subclasses of mammals differ strikingly in their modes of reproduction

1. Prototheria (monotremes) Metatheria (marsupials) The 3 subclasses of mammals differ strikingly in their modes of reproduction Eutheria (placentals)

2. Monotremes – • Lay eggs • Cloaca • No nipples

3. Ovaries larger (relative to body size) than other mammals Oviducts open into common urogenital sinus, similar to reptile cloaca (meaning of name “monotreme”) Milk secreted by glands in skin, licked from tufts of fur at concentrations of glands Testes abdominal, penis is sac in floor of cloaca Young have “egg tooth” like birds to help break out of egg Platypus: 1-2 eggs Echidna: 1 egg Some features of monotreme reproduction

4. Typical platypus reproduction: Egg is fertilized in fallopian tubes before entry to uterus, eventually coated with leather mineralized shell before being laid. But first, uterine wall secretes nutritous secretions which are absorbed by fertilized egg, which grows in size (about 3X). Egg at fertilization = 4 mm, when laid = 12 mm. Egg retained in uterus about 28 days while development proceeds. THEN shell added, egg laid, 10 more days of external incubation. (Eggs sticky, female cradles between stomach and tail.) Lactation about 3-4 months.

5. Similar for echidnas: Only 1 egg, incubates in a pouch where hatching occurs. Young suckle in pouch for about 55 days, when they start to get too prickly! Lactation for about 4 months more.

6. Our friend, the opossum • Young tiny at birth (0.16 g) • Attach to nipples in pouch (marsupium) • Short gestation, longer lactation

7. How opossums do it: Mating season, January – July, 1-2 litters depending on latitude. (2 is typical for Illinois) Egg fertilized in fallopian tubes, also surrounded by a shell membrane (soft) at that time. Egg embeds in uterine wall, absorbs nutritious secretions through membrane and grows. Membrane retained for about 2/3 of gestation (about 8 days). Last 1/3 of gestation (4 days), membrane shed, eggs sink into depressions in uterine wall (has a kind of placenta, but no firm implantation), absorbs nutrients and embryos continue to grow.

8. Gestation totals about 12-13 d. Avg. 13 nipples (some variation), about 7-9 young make it to suckling stage. Fixed to nipples about 50-65 d, about 12% mortality. Lactation continues to a total of about 95-105 days. No continued association after weaning. Rarely live longer than 18 months. In wild, maximum known lifespan was 3 years. Females often get just 1 breeding season, some early-born females may get 2.

9. Eggs slightly larger than in placentals (0.12-0.28 mm vs 0.07-0.15 mm) Uteri separate, but females also have paired (not single) vaginae; new, median canal forms at parturition Young never larger than about 1 g, no matter size of mother Gestation always short as or shorter than length of estrus cycle No invasive placenta Many have pouch, but some only have folds of skin, and a few don’t have anything In males, penis is bifid (forked) like female vaginae Scrotum lies in front of penis, opposite pattern in placentals Some differences (from placentals) found in marsupials

10. Differences in female reproductive tracts

11. Gestation versus lactation Big difference between marsupials and placentals is development of young at birth. Marsupials have very short gestation periods compared to placentals of the same size, but longer periods of lactation.

12. Another way to look at this...

13. Time: conception to weaning Takes marsupial longer than placental to raise young to same size (weaning age)

14. So, which is “better?” Costs: Lactation is most energetically costly period of reproduction, and less efficient means of energy transfer to young. Marsupials eventually raise offspring of similar relative body sizes as placentals, but probably costs them a bit more in terms of time and energy. Constraints: Newborn marsupials need to be able to crawl to pouch or teat, suckle, breathe, digest... More advanced than placental embryo at same stage. But no wings, hooves, or flippers! Flexibility: Very little investment by marsupials in individual offspring at time of birth, can adjust litter sizes, etc.

15. Joey the kangaroo In marsupials, lacation shuts down development of any other fertilized eggs (= diapause) Red kangaroos live in arid regions with unpredictable rainfall. Can become baby factories during good times. Type of milk produced by 2 teats also varies over time (% protein, fat, carbohydrates).

16. Semelparity vs iteroparity Semelparous: only 1 reproductive period per lifetime Iteroparous: multiple reproductive events per lifetime Semelparity is very unusual for mammals, but....

17. The Amazing Antechinus! Small dasyurid marsupial All females give birth within a few days each year (synchrony; Oct = Australian spring) In late Sept, shortly after females mate, all males die! Every year, males go into hormonal overdrive, turn all energy into breeding activities, form aggregations (like leks?) that are visited by females. After 3 weeks of this, makes stressed out, gastrointestinal ulcers, hair loss, stress-induced diseases... Die! Females can store sperm, only receptive during mating period, get pregnant and give birth after all males in population are dead. (males live 1 yr, females mostly 1, 2, very rarely 3)

18. Most mammals are iteroparous, but iteroparity can vary: Monestrous: 1 reproductive event per year. Examples: large mammal with long gestation period, such as white-tailed deer, but also hibernators, such as ground squirrels. Iteroparous over multiple years. Very predictable annual cycles. Polyestrous: many estrus cycles (ovulations) per year. Seasonally polyestrous: multiple estrus cycles, but within limited times of year. Examples are most small mammals, such as voles and mice. Iteroparous within a single breeding season or year. Small rodents and insectivores can enter estrus every 4-5 days during peak season if not mated. Gestation around 21 d, can get pregnant again while lactating (often post-partum estrus), weaning takes about 3-4 weeks... Young can start breeding at about a month of age! Downside: short life. Maybe only 1 year.

19. Reproductive patterns of gray and fox squirrels in Illinois If 2 litters per year, 1 in spring and 1 in late summer. Litter size usually 2-3. Lifespan: gray up to 6 yrs, fox around 7 years.

20. Capital vs Income Breeders Capital breeder: accumulate energy reserves for breeding Income breeder: relies on high metabolic rate, ability to obtain and process energy currently available in environment for reproduction White-footed mouse: litter size and reproduction adjusted to environmental conditions; opportunistic Harbor seal: accumulates fat to help support annual, intense lactation period; predictable

21. General pattern for a placental mammalian reproductive event is: O -> F -> B -> I -> DP -> DF -> Part O = ovulation F = fertilization B = formation of blastocyst I = implantation of blastocyst in uterine wall DP = development of placenta DF = development of fetus Part = parturition (birth) Timing is important! Births should occur so that lactation, the most energetically demanding period, coincides with the most favorable environmental conditions in a seasonal environment

22. For example, red foxes are monestrous. Females come into estrous during late Jan to early Feb, for a short period of 3-4 days. Females within a population are relatively synchronous. (probably to keep those mates honest!) Males are reproductively capable (= active spermatogenesis) for a longer time, around Dec through March or so, that encompasses the time of female receptivity. (probably to be available for any opportunities!) Gest = about 51 d. Mating in winter assures young will be born in late March or April, right at start of “good” season.

23. Other species, such as ground squirrels, have short enough gestation periods that they can wait until the start of spring to initiate reproduction. Hibernators, 7-8.5 months per year underground Males emerge 1st, mid-April, about 2 weeks before females in early May Breeding occurs after females emerge, gest = 26-28 d, young born by late May to early June Because young need to grow, and adults need to fatten up, can only have 1 litter per year 13-liner Franklin’s

24. It’s not smart to just reproduce whenever you feel like it... When particular events or situations such as seasonality, hibernation, or migration constrain when certain reproductive events can occur... ...especially if the time from conception to weaning is longer than the “good” environmental period, or young need to grow to meet the challenges of the “hard” season... ...then some mammals can vary the order and timing of this pattern.

25. Some variations on a reproductive theme

26. Delays in fertilization, implantation, and development are ways used by mammals to help coordinate births with favorable environmental conditions. In delayed implantation, mating and fertilization occurs, but development stops at the blastocyst stage for a time... Blastocyst floats free in uterus, surrounded by protective zona pelucida. Implantation occurs later. Mink Delayed implantation occurs in many carnivores, especially solitary types like large mustelids, pinnipeds, bears, and a few others... Mink in Illinois: mating extends from Jan through March...longer in more northern populations. Gestation is variable, 40 to 75 days depending on when implantation occurs. Births in April – May.

27. Bats show all sorts of patterns. Different species show delayed fertilization, implantation, or development. Some tropical bats are seasonally polyestrous, and show different patterns for different reproductive cycles! Hibernating bats have especially modified the general pattern to their life history. Big-eared bat

28. Notables: • Delayed fertilization • Sperm storage by both males and females • Mating during fall, and also during hibernation! • Can’t wait for reprod activity to start in spring, young need to grow and prep for hibernation, adults need to store fat • Spring torpor slows development, long gestation (50-60 d!)

29. Overall fast-slow continuum Small, short-lived mammals reproduce as continuously as possible to balance short life span, high mortality rate. Tend to be more opportunistic and less strictly seasonal. Larger litters, with young being greater % of female body mass (higher mass-specific metabolic rates). Larger and longer-lived mammals are more selective about timing of reproduction. Larger especially have longer gestation times, which limits flexibility. Some must build up reserves. Thus, use variety of means to vary general pattern of events from conception to birth. Larger investment in individual young (quality more important than number).

30. Precocial young: ungulates, whales, primates Altricial young: rodents, insectivores, carnivores like canids and bears Altricial: can have more young per litter

31. Polyembryony in 9-banded armadillo

32. Record for longest gestation: 22 months (shortest is a bandicoot, 12 days)

33. Enough for 1 lecture...