Reproductive Behavior, Mating Systems, and Parental Behavior PDF

Reproductive Behaviour, Mating Systems and Parental Behaviour Mating associations and parenting behaviours  Overview Thissection is on mating Second,we will discuss mating systems and connected systems per se phenomena....

Reproductive Behaviour, Mating Systems and Parental Behaviour Mating associations and parenting behaviours  Overview Thissection is on mating Second,we will discuss mating systems and connected systems per se phenomena. This will include the First, we will discuss: coverage of examples with: Modes of reproduction. Mammals Reproductive effort, success Canids and investment. Callitrichids Parental care and behaviour, Cricetids including parental investment and speci c forms of care: Birds Maternal, paternal, bi- Anseriformes, mostly parental, and alloparental. Anatids fi  Reminder: Mating or breeding systems One-to-one: Monogamy More on the details of this slide later: But these terms will be used frequently before I give the details. One-to-many: Polygamy One female with many males: Polyandry One male with many females: Polygyny Many-to-many: Network of preferences: Polygynandry* (some-to-some) Promiscuity: Polybrachygamy (true many-to-many) * Human equivalent: Polyamory  Reproduction: Reproductive modes Reproductive behaviour/strategies/systems: Courtship (covered, in sexual selection) Mating Parental behaviour and Parenting Alloparental behaviour  Modes of reproduction I Classi cation according to: 1. Production of gamete: egg, sperm, or both: See next slide 2. Method of fertilization: Internal* or external**. 3. Method of production of the young: Viviparity, ovoviviparity, oviparity, etc. * all caecillians, reptiles, birds and mammals, most salamanders, some frogs and toads ** sh, most frogs and toads, some salamanders fi fi  Modes of reproduction II 1. Gonochoristic (dioecious) mode: Separate male and female individuals. The most common. 2. Hermaphroditic (monoecious) mode: Individuals have both eggs and sperm. Example: Slugs and snails. 3. Parthenogenetic mode: All individuals have ovaries. No fertilization necessary. Rare, not always obligatory. See next two slides. Parthenogenesis !? In parthenogenesis, all individuals have only ovaries and produce only eggs ("virgin birth"): Top minnow, mole salamander (lower right). In some cases, sperm is not required for complete and normal development: whiptail lizard (top right), Cnemidophorus (only females [2 will interact a mock mating], no males » cloning of the female). In other species, sperm is necessary, yet the sperm's genome is not included into the genome of the young: the Amazon Molly (Poecilia formosa). Known cases, some very recently documented: 1. Some shark species: bonnethead sharks (Sphyrna tiburo), zebra sharks (Stegostoma tigrinum), black tip reef sharks (Carcharhinus melanopterus) 2. Blind snakes: brahminy blind snake (Ramphotyphlops braminus); only females exist as far as we know. 3. Komodo dragon (Varanus komodoensis): 2006! 4. American crocodile (Crocodylus acutus): 2023! 5. California condor (Gymnogyps californianus): 2021! Other birds where reported: Turkeys, Chickens, Pigeons, Zebra Finch. More here: https://www.livescience.com/animals/animals-that-have-virgin-births? utm_source=facebook.com&utm_medium=social&utm_campaign=social ow&utm_content=livescience&fbclid=IwAR217ZyLk-wV80MBC5QfhwF6g_sGpMP-5bu6r9UB9hYAsRIExDiO49geQnY fl  Parental care and behaviour De nition 1: Behaviour[s] performed in relation to one's offspring that contribute directly to the survival of the fertilized eggs or offspring that have left the body of the female (Nelson, 1995, 2000). Denition 2: All activities that are directed by an animal towards the protection and maintenance of its own fertilized eggs or offspring or those of a kin. Maternal care or behaviour: parental behaviour performed by the mother (or by extension an other female, i.e. step mother or allomother). Paternal care or behaviour: parental behaviour performed by the father (or by extension an other male, i.e., step-father). Mostly associated with monogamy. Alloparental care or behaviour speci cally: care from a kin other than father or mother. fi fi fi  Parental investment De nition: The extent to which parents compromise their ability to produce additional offspring in order to assist current offspring. Although the investment in the current offspring will increase its chances of survival and reproduction, it may result in a con ict of interest between parents and offspring. fi fl  Reproductive effort Energy and time investment as well as risk taken for breeding. The breeding activity may reduce the reproductive success of the individual. Finding mates, courting, getting access to mates, mating, caring for the offspring: all these activities demand time and energy and often increase vulnerability to predators.  Reminder: reproductive success Is a function of (and can be measured by): number of offspring's born number of weaned individuals number of individuals available for mating  Parental experience hypothesis Example: in rhesus monkeys, mothering seems to require a learning process. Primiparous females lose their infant 55% of the time. The survival rate stabilizes after the 3rd one: 3rd: 78% survival rate after 6 months. 4th: 91% survival after 6 months.  Sex difference (in "priorities") Males: function of how many females are inseminated Females: function of how many eggs are produced The variance in copulatory (and therefore reproductive) success is usually higher for males than for females (Bateman effect) EXCEPT in cases of stable pair bonds (strict monogamy).  Parental care: main theories Parental provision model classical view on parental care parent » offspring Con ict model based on Trivers’s theory (1972) and Alexander's data (1974) parent « (-) » offspring Symbiosis model (more speci cally, mutualism) “transactional” theory parent « (+) » offspring fl fi  Con ict theory According to Richard Alexander (1974), parents should always be favoured in this contest. The parental tness is the priority through "parental manipulation". With time, the cost is higher for the mother, i.e., the cost/bene t ratio is over 1; Example: cats 1-20 days: mother initiates nursing 20-30 days: equal initiation 30+ days: only the kittens initiate These observations are based on the (increase of) "intensity" of the con ict. fl fi fi fl  Issues with the con ict theory Mathematical models (e.g., Parker and the game theory model) do not con rm Alexander’s view. On major problem: how can we measure the intensity of the con ict? Maybe “intensity” is not the best measure of con ict. Many of these models look at species where only one parent is involved, and with only one litter/year. What if multiple paternity? Paternal care? Different litters at different seasons (e.g. rodents)? Last point: sometimes, the competition is between siblings as in Spotted Hyenas (Crocuta crocuta) and many species of birds (e.g., egrets). In many cases, this involves siblicide (more speci cally, fratricide, or killing of brothers or sisters). fi fl fl fl fi  Symbiosis (mutualistic) theory Alberts & Gubernick: bidirectional exchange ("transactional view"). Study looked at urogenital licking by mothers in rats (common in rodents and carnivores). Radioactively labelled water (with tritium) injected to rat pups. When urethral ligation: water not detected in mothers. Conclusion: pup urine is source of water for the mother. Mother gets 2/3 of the water passed to the pups by her milk. Rat milk: 73% of water. Peak of transfer is at peak of milk production / consumption. What if water is given? --> Friedman, Bruno & Alberts (1981): water is not enough. The urine is source of electrolytes (salts) such as sodium.  Male vs. female care: 3 views Certainty of paternity hypothesis (50% of a father's genes are in the offspring). If high, will care for the young... if low, won’t... (that is, if the male does not kill the progeny: e.g., lions). Paternity is most uncertain in species with internal fertilization: In theory, species with external fertilization (amphibians, sh): more paternal care should be observed (e.g., sticklebacks, seahorses, pipe sh). Species with internal fertilization (most reptiles, birds, mammals): more maternal care (certainly applies to mammals). Other factor: mating system. Monogamous species show (even in mammals) more paternal care. If mating is exclusive between the 2 parents, this makes sense. fi fi  Gamete order hypothesis (sperm or eggs) The last parent to release gametes gives the parental care This theory favours the desertion of offspring ASAP Major limitation: fertilization mode (internal or external). In mammals internal fertilization is the rule. Females care more by default: they can't leave the embryo. Gestation is the factor. In amphibians and sh, external fertilization is the rule. Males tend to care more for the progeny (if there is any parental care). Association or proximity hypothesis Proximity of adults and offspring's determines parental behaviour. The internal - external fertilization limitation applies here as well. Gestational (most mammals) versus non-gestational development. Territorial males » paternal: Territoriality guarantees their proximity. fi  Paternal care (species-level) Rare in sh, amphibians, reptiles, and mammals. Common in birds, although often in the context of biparental care. How is paternal care de ned in amphibians and Amphibians and reptiles: reptiles? Here are some criteria: 1. Turtles: 1% 1. Nest creation and nest attendance 2. Lizards: 1.3% 2. Nest or egg guarding 3. Snakes: 2.8% 3. Egg, larval, hatchlings, froglet transport 4. Frogs/toads: 6% 4. Egg brooding 5. Salamanders: 20% 5. Feeding the young 6. Crocodylians: 100% 6. Guarding or attending the young Information from Vitt and Caldwell, 2014 fi fi  Paternal care is often associated with monogamy or polyandry The Northern Jacana: an example of strong paternal care in males The females: typical male bird attributes. are polyandrous are responsible of territorial protection have the dominant role in courtship are of large size The males: are of small size are involved in nest building are involved in incubation/brooding are involved in the defence of the chicks  Alloparental care Denition: care given by other individuals than the parents. Can be called more speci cally “allomothering” or “aunting” (when females are involved). Frequent in cooperative breeders (mammals living in extended “families”, in birds), in monogamous species or matrilineal polygynous species. Can potentially serve two functions: From the kin selection perspective: Non-breeding individuals take care of individuals of their own “family” (i.e., individuals sharing genes). From parental experience perspective: Gives experience for when they become parents themselves later. fi fi  Helpers Helpers: kin helping to raise the young. Usually females (called "allomothers" or "aunts"). Often sporadic (depending on resource availability). Example: red foxes (Vulpes vulpes): daughters from the previous year or "aunts" stay for one more season to assist their mother. Characteristics of helpers: why don’t they disperse? Risks of nding a suitable territory Risks of nding a mate Risks of successful reproduction They stay to help the mother but also because dispersal would be too risky for themselves. fi fi  Helping in canids In red foxes (Vulpes vulpes): daughters from the previous year. Facultative. Inwolves (Canis lupus): became a “social system” or unit (the pack, i.e., an extended family). Obligatory (if true pack structure) or facultative (when parent-young immediate family groups are formed, e.g., Arctic Wolf) In coyotes (Canis latrans): Intermediary and exible system. fl  Patterns of paternal care Paternal care is common in species with: Monogamy (e.g., many birds, some mammals, amphibians (e.g., lungless salamanders), reptiles, sh). Cooperative breeding (associated with monogamy). Paternal care is usually associated, at least in birds and mammals, with biparental care (care by both parents): } 3% of mammals Those numbers vary from source to source 70% of birds fi  Evaluating male investment: criteria in wild canids 1. Grooming 5. Guarding (passive) 2. Transporting/Carrying/ 6. Baby-sitting Retrieving 7. Playing 3. Feeding (males bring food to young or 8. Care to female (usually regurgitate) bringing food) 4. Defending (active)  Notes of species differences Even within one taxon, patterns of paternal care vary greatly (see next slide, the comparison of 21 species of Canids; from Gadbois, 2002, adapted from Asa, 1997; Asa & Valdespino, 1998; Kleiman & Malcolm, 1981; Malcolm, 1985). Other examples: The African hunting dog (Lycaon pictus) and many callitrichid (marmosets, tamarins) monkeys are involved in all the categories above. They basically match the mother and sometimes more, except for lactation.  fe or g ng ng ev ng g in g Paternal care in Canids ng g tti in in ar g di tri yi in i rd om in -s i C re arr en e ed ay ua al f by ro ef Pl C Fe m G Ba G D Maned wolf (Chrysocyon brachyurus) ✔ Corsac fox (Vulpes corsac) ✔ Swift fox (Vulpes velox) ✔ Kit fox (Vulpes macrotis) ✔ Cape fox (Vulpes chama) ✔ Pampa fox (Pseudalopex gymnocercus) ✔ Andean fox, culpeo (Dusicyon culpaeus) ✔ Raccoon dog (Nyctereus procyonoides) ✔ Red fox (Vulpes vulpes) ✔ ✔ Red wolf (Canis rufus) ✔ ✔ Arctic fox (Vulpes/Alopex lagopus) ✔ ✔ ✔ Fennec (Fennecus/Vulpes zerda) ✔ ✔ ✔ Dhole (Cuon alpinus) ✔ ✔ ✔ Crab-eating fox (Cerdocyon thous) ✔ ✔ ✔ ✔ Bush dog (Speothos venaticus) ✔ ✔ ✔ ✔ Bat-eared fox (Otocyon megalotis) ✔ ✔ ✔ ✔ ✔ Black-backed jackal (Canis mesomelas) ✔ ✔ ✔ ✔ ✔ ✔ Golden jackal (Canis aureus) ✔ ✔ ✔ ✔ ✔ ✔ Coyote (Canis latrans) ✔ ✔ ✔ ✔ ✔ ✔ Wolf (Canis lupus) ✔ ✔ ✔ ✔ ✔ ✔ African Wild dog (Lycaon pictus) ✔ ✔ ✔ ✔ ✔ ✔ ✔ ✔  From parental care to mating system: The case of cooperative breeding Cooperative breeding is rare in mammals (1%); Lukas & Clutton-Brock, 2017). Lukas & Clutton-Brock (2012) identify 34 mammalian species that t a conservative de nition. It is the most common in 3 orders of mammals: Carnivores: The Canidae* (canids) and Herpestidae** (mongooses/ meerkats), arguably the Coati (Nasua narica) Primates: The Callitrichidae (marmosets and tamarins) Rodents: A few family, see next slide * Canis (wolves), Lycaon (African wild dogs), Alopex (arctic fox) ** Meerkat, Banded mongoose, Dwarf mongoose fi fi Rodents engaged in cooperative breeding (usually only some species within these families and genera) Bathyergidae: Mole-rats (the only true eusocial mammals) Castoridae: Beavers Hystricidae: Porcupines Terrestrial Sciuridae: Ground squirrels (Spermophilus genus), prairie dogs, some would include alpine marmots in this group (Marmota genus). Muridae/Cricetidae: Mice and rats. Including Microtus and Peromyscus (see below), Meriones (gerbils). Cooperative breeding in birds About 3%-8% of birds (a small fraction of the monogamous species). It is widely distributed all across the bird class (taxon). Too many to list here. The majority of species are in Australia and South Africa. It is most common in the following groups (taxa): Coraciiformes: King shers, bee-eaters, etc. Piciformes: Woodpeckers, etc. (e.g. Acorn woodpecker) Passeriformes (this is a huge group, also referred to as passerines) such as corvids (two local species: American crow* and Canada or grey jay**), the invasive house sparrow (Passer domesticus), the bobolink*, and many others (wrens, starlings, ycatchers, etc). * Brown, 1987 ** Waite & Strickland, 1997 fi fl Mating systems  Reminder: Mating or breeding systems One-to-one: Monogamy One-to-many: Polygamy One female with many males: Polyandry One male with many females: Polygyny Many-to-many: Network of preferences: Polygynandry* (some-to-some) Promiscuity: Polybrachygamy (true many-to-many) * Human equivalent: Polyamory  Polygamy: polygyny One male mating with and controlling access to many females. By far the most common form of polygamy. Types: Resource-defence Female-defence Male-dominance: females are choosing. Scramble: males searching for mates without competition  Polygamy: polyandry One female mating with and controlling access to many males. Uncommon system. Often in combination with male polygyny or an alternative to monogamy (e.g., some social canids). Associated with sex role reversals, with males doing most of the parental care. Types: Resource-defence Female-access  Examples of polyandry Birds: polyandry is more common in birds. Examples: some hummingbirds, spotted sandpipers, Galápagos hawk, phalaropes, jacanas, rheas, etc. Mammals: A few "New World" monkeys (although arguable), African Wild Dog (if not monogamy).  Polygynandry & promiscuity Males and females have multiple mates. Two types: Polygynandry:non-random choice and pairing of males and females; polygynous males with polyandrous females. Example: chimpanzees. Promiscuity (polybrachygamy): random choice and pairing of males and females; both sexes have multiple partners. Examples: chimpanzees; many "monogamous" primates (e.g., gibbons, siamangs, tarsiers) may actually t this system better. fi  Alternative mating strategies Used when males are unsuccessful at getting access to a mate (in monogamous or polygynous species). Forced matings or copulations ("rapes"): Common in birds? Documented example: Mallard ducks Surreptitious matings or kleptogamy (sneak mating): Mimicry (of females) in male bluegill sun sh (Dominey, 1980). Bullfrogs: satellite positions and croaking. Deer, wolves, etc.: opportunistic beta or defeated individuals take advantage of distracted males. fi  Types of monogamy 1 Genetic monogamy: DNA analysis con rming the mating / pair bond between a male and a female. Sexual or mating monogamy: exclusive male-female relationship based on sexual interactions. Social monogamy: social living arrangement between a male and a female (e.g., coyotes). fi  Types of monogamy 2 Mating system or social system? Monogamous social system = social monogamy. Monogamous mating system = monogamous sexual and genetic relationships.  Monogamy: 7 criteria adapted from Poole (1985) and Dewsbury (1988) 1. Reduced sexual 5. Exclusion of strangers dimorphism (non-kin) from the family 2. Exclusivity of mating 6. Reproductive suppression 3. Pair bond 7. Incest avoidance 4. Biparental care (i.e., paternal care)  Reduced sexual dimorphism and reproductive variance Reproductive Mating system Body size Maturation variance Monogamy Equal Equal Equal Polygyny Male larger Males slower High in males In principle higher in Polyandry Females larger Females slower females  Exclusivity of mating Means: number of (sexual) partners in time. Exclusivity: applies to copulation & paternity. Temporal dimension: Simultaneously: Exclusivity factor (unfaithfulness vs. faithfulness). Serially: Serial monogamy Biological measures: genetic markers (if inheritance pattern known) protein electrophoresis (exclusive method) DNA ngerprinting (expensive) fi  Pair bond The nature of the association and interaction(s) Spatial proximity (shared territory / home range)? joint nesting, denning... shared home range joint travel Frequency: continuous or discreet associations? Duration: length of the pair bond Examples: large spectrum from copulatory-restricted bond (gibbons) to "superfaithfulness" (geese).  Biparental (+) care Male/female involvement and investment (time and energy) is high and often equal. Sometimes alloparental care (cooperative breeding). Continuum: Helpers (facultative; one sex [females only]), to Extended, multigenerational, permanent families.  Other criteria Exclusion of strangers from the family: non-kin are rarely tolerated. Fits with kin selection theory. Immediate family or extended family systems. Reproductive suppression of non-breeding individuals or subordinates (when a dominance hierarchy exists). Non-breeders are usually helpers. Incest avoidance: does not apply to all species, but the "incest taboo" is often observed.  Monogamy vs. polygamy About 90% of birds are monogamous. Grif th et al (2002): Genetic monogamy is less than 25%? Only 4% of mammals are monogamous. Most species with paternal care are monogamous although paternal care is also found in polygynous species such as zebras and Indian langurs. Monogamy is more likely to be observed when resources are scattered or shelter/nest sites are scarce (in species where monogamy is "facultative"; see below). fi  Monogamy or "monogamy" Monogamy seems to be, no more and no less, a “preference” for a speci c mate (Sue Carter). Manymonogamous species have indiscretions ("in delities"). Example: gibbons, wolves, voles. Gallivanting (Barash, 1981) or extrapair copulations and common in males as well as females. Many species are actually “opportunistically polygamous” (as opposed to strictly monogamous or promiscuous). Important factor: mate “monopolization” or control. fi fi  Taxonomies of monogamy 1* (mammals) Facultative: paternal Obligate: more cohesive, investment is low (sometimes paternal care, extrapair absent), loose association, mating very rare, occasional occasional polygyny. polyandry. Extreme facultative Extreme obligate Group size = J J J J J J Group 1 2 3-6 SA >4 SA SA >6 SA composition: sex A A and juveniles (J), subadults (SA) and adults (non- breeding; A) Temporary Permanent Permanent Solitary Pair family nuclear family extended family * Kleiman (1977, 1981) ♀︎♂︎♀︎♂︎ ♀︎♂︎♀︎♂︎♀︎♂︎ Taxonomies of monogamy 2* (mammals) Dimension 1 (spatial): Dimension 2 (temporal): Territorial Serial Female-defence Permanent Dominance-based * Wittenberger (1979, 1981) Note: from and exhaustive classi cation of vertebrate mating organization; applies to other systems as well General classi cation Spatial classi cation Temporal classi cation Territorial Serial Monogamy Female-defence Permanent Dominance-based Territorial Successive Polygyny Harem Simultaneous Territorial harem Territorial Successive Polyandry Non-territorial Simultaneous Broadcast Promiscuity (polybrachygamy) / Overlap polygynandry Arena Hierarchical fi fi fi fi Taxonomies of monogamy 3* (mammals) Grade I: male and female defend common territory but offspring (usually) leave after weaning. Example: Red foxes, elephant shrews, tree shrews, klipspringer. Grade II: adults are permanently paired but the dispersion of the young is (often) delayed. Examples: coyotes, beaver, some marmots. Grade III: rank-determined monogamy (multi-male/ multi-female groups): callitrichids, wolves, African wild dogs, dholes. * Poole (1985)  Elephant shrew (Rhynchocyon petersi) Common treeshrew Klipspringer (Oreotragus oreotragus) (Tupaia glis) Social and mating systems taxonomy in wild canids Nyctereutes procyonoides: Raccoon dog The only hibernator in canids Raccoon dog (Nyctereutes procyonoides) Fennecus/Vulpes zerda: Fennec Fennec kit (baby) Lycaon pictus: African Wild Dog Speothos venaticus: Bush dog Cuon alpinus: Dholes  Taxonomies Mating / parental / alloparental / social system Fox Kleiman Hunting Territory Poole 1985 Family bond Pair bond Paternal care 1975 1977 pattern Dispersion Solitary Transient Temporary Paternal Male and female hunters family pair. investment is defend common Some paternal low, loose territory. Type I Grade I care. association. O spring leave after weaning. Facultative Occasional Solitary-social Temporary Adults are polygyny. Young’s hunters(transit family permanently dispersion often Type II Grade II ional type) paired.Someti delayed. mes helpers. Social hunters Permanent Permanent Cohesive Status (rank)- (pack type) family. pair or pack paternal care. determined Type III Grade III Obligate structure. monogamy Extra-pair (multi-male, * Clear-cut Only alpha mating very multi-female see next slide dominance animals rare. groups) Type IV - - hierarchy breed. ff * Note: Fox (1975) recognizes that the Dhole "exempli es a further evolution of canid social behaviour, where the term "clan" is appropriate for such a large group sharing the same range but rarely hunting together" and goes on saying that "It therefore constitutes a Type IV canid social class, the clan (analogous to the baboon troop)". fi  Fox Kleiman Poole 1985 Species / genera 1975 1977 Nyctereutes procyonoides: raccoon dog Type I Grade I Fox-like canids (vulpines): Urocyon cinereoargenteus (grey foxes), Vulpes/Alopex lagopus (Arctic fox), many Vulpes foxes (except V. vulpes and corsac). Facultative Canis genus (except Canis lupus): Dingo (Canis familiaris dingo), red wolf Type II Grade II (Canis rufus), coyote (Canis latrans), and all four species of jackals. Some vulpines: Vulpes vulpes (red fox) and Vulpes corsac (Corsac fox). Canis lupus: Wolf Type III Grade III Obligate Lycaon pictus: African Wild Dog (or Painted Dogs) Speothos venaticus: Bush dog Type IV - - Cuon alpinus: Dholes (Indian Wild Dogs)  Summary for Canids: Emergent social and reproductive characteristics Monogamy IF EF CF Parental care: Paternal care Alloparental care: From occasional helpers to true cooperative breeding. Family systems: Immediate or nuclear family: Foxes, Coyotes. Extended family: Wolves, African Wild Dogs. Congregation of families (clan system): Dholes.  From mating system to social system: Temperament and relationships with siblings Personalities Play Aggression Prototype species (Fox 1975) (social) (sibling) Most vulpines (fox-like canids) Monomorphic + +++ Most canines: Coyote Oligomorphic ++ ++ Jackals (4 sp.) Wolf African Wild Dog Bush dog Polymorphic +++ + Dhole Overview of monogamy in mammals  Monogamy in mammals 1 Marsupialia (marsupials): a few species Macroscelidae (elephant shrews): a few species Chiroptera (bats): false vampire bats Lagomorpha: hares, rabbits, pikas: a few species Rodentia (rodents): Sciuromorphs (squirrel-like): Castoridae (beavers) Myomorphs (mouse-like): Some voles & mice, gerbils, spiny mice. Hystricomorphs (porcupine-like): ?  Myomorpha examples: Peromyscus Peromyscus genus: The deer mice 55 species (Nowak 1991); 2 species common in the Maritimes (+ QC, ON) Peromyscus maniculatus: Common deer mouse Peromyscus leucopus: White-footed mouse 2 only are monogamous in the genus: Peromyscus polionotus: Old eld mouse Peromyscus californicus: California deer mouse fi POLYGAMOUS Peromyscus maniculatus: Deer mouse Peromyscus leucopus: White-footed mouse MONOGAMOUS Peromyscus polionotus: Old eld mouse Peromyscus californicus: California deer mouse fi Deer mouse (P. maniculatus)  Old eld deer mouse (P. polionotus) fi  Myomorpha examples: Microtus Microtus genus: The common voles 67 species (Nowak 1991)*; 2 species in the Maritimes (QC, ON as well) Microtus pennsylvanicus: Meadow vole (very common) Microtus chrotorrhinus: Rock vole or yellow-nosed vole (very uncommon) 2 only are monogamous in the genus: Microtus ochrogaster: Prairie vole Microtus pinetorum: Woodland vole * The ITIS database identi es 62 species: https://www.itis.gov/servlet/SingleRpt/SingleRpt?search_topic=TSN&search_value=180296#null fi POLYGAMOUS Microtus pennsylvanicus: Meadow vole Microtus chrotorrhinus: Rock vole MONOGAMOUS Microtus ochrogaster: Prairie vole Microtus pinetorum: Woodland vole Spiny mouse (genus Acomys)  Monogamy in mammals 2 Cetacea (whales, porpoises, dolphins): a few species } Perissodactyla (odd-toed ungulates) such as rhinoceros, horse, ass, { Ungulates zebra: a few species Artiodactyla (even-toed ungulates) such as pigs, hippopotamus, deer, gazelles, buffalo, sheep, goats, etc.: a few species Carnivora (carnivores): Canidae: most species (except: raccoon dog and some South American canids) Viverridae (civets, genets, mongooses, etc.): dwarf mongooses, +? Hyenidae (hyenas): brown hyenas, aardwolves?  Dwarf mongoose (Helogale parvula) The dwarf mongoose is the smallest African carnivore, with a size of 20 to 30 cm long.  Monogamy in mammals 3 Primates: Apes Great apes: none Lesser apes: Hylobatidae (gibbons and siamangs), although minimal paternal care. Monkeys callitrichids (marmosets and tamarins) titi monkey (genus Callicebus) night or owl monkey (genus Aotus)  Marmosets Geoffroys marmosets Baby pygmy marmosets Marmosets Marmosets  Callitrichids (marmosets & tamarins): a diverse group Black-headed Marmoset, Callithrix (Mico) Subgenus Callithrix - Atlantic marmosets nigriceps Common Marmoset, Callithrix (Callithrix) jacchus Marca's Marmoset, Callithrix (Mico) marcai Black-tufted Marmoset, Callithrix (Callithrix) Black-tailed Marmoset, Callithrix (Mico) melanura penicillata Santarem Marmoset, Callithrix (Mico) Wied's Marmoset, Callithrix (Callithrix) kuhlii humeralifera White-headed Marmoset, Callithrix (Callithrix) Maués Marmoset, Callithrix (Mico) mauesi geoffroyi Gold-and-white Marmoset, Callithrix (Mico) Buffy-headed Marmoset, Callithrix (Callithrix) chrysoleuca aviceps Hershkovitz's Marmoset, Callithrix (Mico) Buffy-tufted Marmoset, Callithrix (Callithrix) aurita intermedia Subgenus Mico - Amazonian marmosets Satéré Marmoset, Callithrix (Mico) saterei Rio Acari Marmoset, Callithrix (Mico) acariensis Subgenus Callibella - Roosmalens' Dwarf Manicore Marmoset, Callithrix (Mico) Marmoset manicorensis Roosmalens' Dwarf Marmoset, Callithrix Silvery Marmoset, Callithrix (Mico) argentata (Callibella) humilis White Marmoset, Callithrix (Mico) leucippe Subgenus Cebuella - Pygmy Marmoset Emilia's Marmoset, Callithrix (Mico) emiliae Pygmy Marmoset, Callithrix (Cebuella) pygmaea fl Titi monkeys (genus Callicebus) Red Titi (Callicebus cupreus discolor)  Titi monkeys RIO DE JANEIRO, Brazil (June 23, 2002 2:32 p.m. EDT) - Scientists working in Brazil's central Amazon have discovered two new monkey species that are about the size of small cats, Conservation International announced Sunday. The monkeys were discovered by Marc Van Roosmalen, a Dutch scientist working at Brazil's National Institute for Amazon Research in Manaus, 1,800 miles northwest of Rio de Janeiro. Van Roosmalen works in a little-explored region of the Amazon near the con uence of the Madeira and Tapajos rivers. Full scienti c descriptions of the monkeys, Callicebus bernardi and Callicebus stephennashi, were published by the peer-review journal Neotropical Primates. fi fl Owl monkey (genus Aotus)  Anseriformes Waterfowl: ducks, geese, swans, etc. Fowl, wildfowl, gamefowl: Galloanserae or Galloanseres Magpie goose (Anseranas semipalmata) Landfowl Waterfowl Galliformes Anseriformes Pheasants, quails, grouse, turkeys, peafowl, Ducks, geese, swans, screamers, guineafowl, junglefowl (“chicken”), ptarmigan, partridge, etc. magpie goose.  Thereare three families of Anseriformes: Anhimidae (screamers, 3 species) Anseranatidae (magpie-geese; 1 species) Anatidae (all others: ducks, geese, swans, etc; 174 species and 43 genera)  Monogamy in birds: Reminder Monogamy, at least “mating monogamy” is believe to be the “rule” in about 90% of bird species (Lack, 1968). Genetic monogamy may just be at 25% of species (Grif th et al., 2002) Paternal care in bird species: 70% Usually associated with biparental care (as with mammals) Monogamy in birds can be: Serial or seasonal Perennial or long-term (50% of all orders and 21% of all families) fi  Mating systems in Anseriformes Polygyny: Magpie goose, maybe opportunistically. More likely to occur in captivity, especially if the sex ratio favours it (harem polygamy). Promiscuity: Maccoa, Musk, African Comb and Muscovy ducks; Black swan. Forced extra-pair copulation or FEPC (a “mixed” reproductive system): Dabbling ducks, pochards, stiff tails. Monogamy: 3 sub-types 1. Perennial (long-term): Mostly swans and geese. 2. Seasonal or annual without re-pairing: Dabbling ducks and pochards. 3. Seasonal or annual with re-pairing: Rare, but found in shelducks and seaducks.  Monogamy in Anseriformes 93% of anatids are monogamous. 7% are polygynous / promiscuous. There is no polyandry. So this is a very homogenous group, like Canids and Callitrichids  The paradox But… in principle, they should be polygynous based on known correlations with other bird groups, e.g., 1. The young are highly precocial and imprint. Same in Galliformes (pheasants, quails, chickens, etc) but those are all polygamous. 2. Pair formation has no temporal or spatial contiguity with the breeding areas: They pair way before mating (months before) and far away from the breeding grounds. 3. They are the only bird taxon where females are more philopatric than males, meaning they are very faithful to natal areas.  Mating systems of the major groups (tribes) * long-term monogamy = perennial monogamy TRIBES Common name Mating system Dendrocygnini Whistling ducks Long-term monogamy (perennial) Anserini Geese and swans Long-term monogamy (perennial) Merganettini Torrent duck Long-term monogamy (perennial) Tadornini Shelducks and shelgeese Long-term monogamy* and seasonal monogamy Anatini Dabbling ducks Seasonal monogamy and some long-term monogamy Aythyni Pochards Seasonal monogamy Mergini Sea ducks Seasonal monogamy with some re-pairing Oxyurini Stiff-tailed ducks (e.g., ruddy ducks) Polygynous, some seasonal monogamy From Baldassare and Bolen, 2006; adapted from Orange & Sayler (1992) and Johnsgard (1978)  Other differences with other bird taxa Malesdo not take part in the incubation (except in the magpie goose, the whistling ducks, and the black swan). Males typically abandon the female between when incubation starts, or halfway (i.e., 2 weeks into the process). Some dabbling ducks species (9) in the Southern Hemisphere provide some paternal care, but no incubation. Importantnote: Species with long-term monogamy are more likely to provide extensive paternal care. This is obvious in the anserini (geese and swans). But… only the black swan male incubates.  Reasoning the paradox Ifmales are free of signi cant paternal care… why do they limit their reproductive variance (i.e., mate with more females)? So polygyny should be expected (yet, it accounts for only 7% of the species), not monogamy. In ducks: The male is essential to the early post-mating stages (egg production). Females are philopatric, so males can’t follow more than one female to different breeding sites. fi Non-monogamy in waterfowl * less certain; picture in the domestication section Anseranatidae or Magpie geese (Anseranas semipalmata): Trios (polygynandy). One male, two females, and “cooperative breeding” with combined brood. Grey-sidedcomb duck (African comb duck; Sarkidiornis melanotos): Polygynous harems. Ruddyduck (Oxyura jamaicensis): Mixture of monogamy, polygyny and promiscuity (polybrachygamy). Maccoa duck (Oxyura maccoa): Polygynous Musk duck (Biziura lobata): Promiscuity (polybrachygamy) Muscovy duck (Cairina moschata): Promiscuity (polybrachygamy)*  Perennial monogamy Also called “long-term monogamy”; may be associated with “super-faithfulness” (a term used by Lorenz). Common in geese and swans: Mate delity 92-100% (Black, 1996) Contrary to ducks, at migration time, geese and swans are not fully grown. The young often stay in the group of the parents. Geese and swans are larger than ducks, so males can actually make a signi cant difference against predators at nest sites. Ducks instead have solitary and cryptic females: So the strategy is completely different. Female ducks are also more likely to conceal their nests. fi fi  Divorce in perennial monogamy Barnacle geese (Branta leucopsis): 40% have more than one partner (1-4 mates) Pair bond duration: +/- 4.70 years Some together for 10+ years, up to 19 years. Annual divorce rate: less than 2% Greylag geese (Anser anser): Annual divorce rate:10.5% Almost 30% of pairs eventually divorce.  Cooperative breeding and brood amalgamation in waterfowl Brood amalgamations or cooperative brood-rearing is common in colony birds. Some semi-precocial bird species do crèching (forming a crèche): Penguins, cormorants, pelicans, etc. This happens when the parents leave to go feed. Types in waterfowl: Adopting: Female or pairs accepts foster young. Kidnapping: Aggressive take-over of the young from an other female. Crèching: One or a few adults collect and care for many young that are unrelated. Gang-brooding: Several parents join together with their brood: https:// www.youtube.com/watch?v=bR5isRRfjjM Canada goose (Branta canadensis) and gang brooding About 50% use biparental care exclusively, and 50% use gang brooding (Connover, 2009). Behaviour learned as an adult. Asgeese get older, they are more likely to use gang brooding. The system is not kin-based. Genetic relatedness is not a factor. The Canada goose is the top gang-brooder in geese (few other species do this).  Canada goose (Branta canadensis) and nannies (babysitters): Form of crèching Some Canada geese will act as nannies or babysitters. This is a form or alloparental care and is considered “reciprocal cooperation” (Riedman, 1982). But also: Greylag geese (Anser anser) goslings may pick a foster family within a few days of hatching. They get themselves adopted by other geese! Why would you not choose your own — best — parents!?* From https://expressdigest.com/nanny-goose-leads-51-goslings-for-a-swim-in-canada/ * Komdeur, Kleefsman, Kalmbach & Loonen, unpublished data  GROUP-SIZE and POPULATION REGULATION: How mating systems and social systems interact with each other  A few de nitions... Group: any social unit in gregarious and social mammals and birds. Pack (canids), troop/band (primates), pride (lions), herd (ungulates) Mated pairs (parents) and dependent offspring are not usually considered a "social group", but rather a family. Extended families (wolves, dholes, lycaons, marmosets, tamarins) are considered social groups. They are usually composed of more than two generations, uncles, aunts, etc. Such animals are usually referred to as "cooperative breeders". Population: group of organisms of the same species in a particular place. fi  Models Wynne-Edwards “group selection” model Selye's model: general adaptation syndrome (GAS) Calhoun's data on overpopulation Christian's model of population regulation Sapolsky’s data on dominance / subordinance  Factors in demographic regulation: Population growth can be regulated by external factors or internal factors. We will focus on intrinsic factors: Behavioural mechanisms (Wynne-Edwards, Calhoun) Physiological mechanisms (Selye, Christian, Sapolsky) Reproductive strategies are relevant to this issue: the r/ K dichotomy (next slide) is actually a continuum.  K selected species r selected species Typical example: Proboscidians (elephants) Myomorphs (mouse-like rodents) Typical environment: Stable, e.g., tropics Unstable, e.g., polar regions, mountains Typical climate: Constant and/or predictable Variable and/or unpredictable Body size: Large Small Development: Slow Fast Life span: Long, usually > 1 year Short, usually < 1 year Iteroparity or repeated reproduction (young at Reproduction: rate Semelparity or single reproduction (young all at once) intervals, successive bouts) Reproduction: age Delayed reproduction Early reproduction O spring quantity (#): Low High O spring quality: High; E ciency Low; Productivity Parental care: Extensive Minimal or nil Parental investment: High Low Low, predictable, density-dependent. No High, catastrophic, density-independent. Yearly Mortality rate: recolonization necessary. recolonization. Competition (intra/inter): High Low/lax; variable Home rang or territory: Yes None or less obligatory or de ned. ff ff ffi fi  Reproductive strategies Reptiles, birds and mammals tend to be K-selected (with exceptions, e.g., many mouse-like rodents). Amphibians are generally r-selected (with some exceptions, e.g., some salamanders). Fish span the range of the r-K continuum. Pipe sh / seahorse: strongly K-selected. Killi sh, minnows, etc.: strongly r-selected. fi fi Internal and external limiting factors and carrying capacity of the environment: Density-independent factors: climate, food, res, oods, etc. Some of these may be modi ed by population density. These factors provoke random uctuations. Will affect mainly r-selected (opportunistic) species. Density-dependent factors: competition (inter or intra), parasitism, disease, predation, shelter availability, food supply. Will affect mainly K-selected (sedentary) species. fi fl fi fl  Mechanisms and their “timing” Suppressive or inhibitory mechanisms in groups (and populations): Behavioural inhibition / suppression Physiological inhibition / suppression Temporal variables: Preconception (e.g., psychological castration in males, psychological contraception in females) Postconception (e.g., psychological abortion in females)  Summary of variables and mechanisms: BEHAVIOURAL PHYSIOLOGICAL Intrasexual aggression Puberty delay Reduced attractiveness Ovulatory suppression Preconception Reduced sexual initiative Luteal insu ciency Mate guarding Harassment of mating Infanticide Implantation block Maternal neglect * Induced abortion Poor provisioning Impaired fetal growth Postconception Inadequate alloparental resources Resorption Induced premature birth * Sometimes called "aggressive neglect" Depressed lactation From J. A. French (1997). Proximate Regulation of Singular Breeding in Callitrichid Primates. In N. G. Solomon and J. A. French, Cooperative Breeding in Mammals. Cambridge. Inspired by Kleiman (1980). ffi  Causes and mechanisms Population and group self-regulation: competition with conspeci cs? inter-speci c competition? (mal)adaptation to environmental constraints? Increase in competition (intra or inter-speci c) and environmental constraints >>> increase in deaths, emigrations, decrease in birth rates, etc. But what about the mechanisms? (see next slides) fi fi fi  Behavioural mechanisms 1 Epideictic displays: e.g., ocking (Wynne-Edwards, 1962). Behavioural mean to assess population density Voluntary homeostatic mechanism to inhibit reproduction. Other type of display: epigamic (for courtship purposes) Territory size modulations: expansion or shrinkage of territorial in uence. Dominance hierarchies: behavioural regulation? physiological regulation? psychophysiological regulation? fl fl  Behavioural mechanisms 2 Overpopulation and social pathology (Calhoun, 1962, 1973) » Behavioural sink, i.e., formation of withdrawn groups. In mice: piles, ghts, popcorn effect. Social chaos. Hypersexuality, homosexuality, cannibalism. Somewhat similar effects in humans although culture dependent (e.g. cities in North America and Japan) or social class dependent (high density often = poverty). In hunter-gatherer societies: delayed onset puberty, prolonged lactation and preferential female infanticide. Overpopulation: triggers reproductive inhibition and dysfunctions. fi  Physiological mechanisms 1 Dealing mainly with the HPA axis (hypothalamo-pituitary- adrenal) and its adrenocortical output. Selye (1950) and the general adaptation syndrome (GAS): Stress » Hypothalamus » CRH » anterior pituitary » ACTH » adrenal glands » glucocorticoids (cortisol or corticosterone) Christian (1959): Agonistic interactions >>> prolonged psychological stress >>> exhaustion of the adrenal glands >>> disease >>> death  Physiological mechanisms 2 Christian (1978): Suppression or inhibition of: immune response in ammatory response growth and sexual maturation spermatogenesis ovulation lactation Some of these effects persist from one generation to the other despite a return to normal population density: Epigenetics… fl  Physiological mechanisms 3 Data from deer, rats, mice and woodchucks seem to support this regulatory mechanism. The stressor is not density, but the level of agonistic behaviours (from competition for limited and limiting resources). Other mechanism: Pheromones Well documented in mice (see next slide) Generalizable to most macrosmatic mammals  Pheromonal effects (rodents) Bruce effect (1959): the smell of a strange male causes a pregnancy block (prevents implantation) or even abortion in females. This effect could account for lower birth rates. Bronson effect (1971, 1979) showed that the urine from stressed mice will produce an adrenocortical response in naive mice. Females grouped together release a pheromone that delays sexual maturation in other females. This delay has been provoked in wild mice in the eld by using lab female urine from high density populations (Drickamer, 1974). Smell from a mature male accelerates sexual maturation of young females (Vandenbergh, 1969). fi  Problems with these studies: Laboratory populations: densities unrealistically high, emigration is prevented, etc. Natural environment studies: factors dif cult to control. Regulatory mechanisms: Evolved for group / population control purpose? Is stress (Selye, Christian, Calhoun) adaptive? Did it evolve as a regulatory mechanism? fi  Group selection vs kin selection? Group selection (interdemic selection) from Wynne- Edwards (1962): Not favoured among modern behavioural scientists because of the following voluntary behaviours he thought were fundamental: Prudent predation Reproductive restraint Kin selection could be a solution: the animal sacri ces its reproductive output if the survival of the group (kin) is ensured. fi