Semelparity and iteroparity are two contrasting reproductive strategies available to living organisms. A species is considered semelparous if it is characterized by a single reproductive episode before death, and iteroparous if it is characterized by multiple reproductive cycles over the course of its lifetime. Iteroparity can be further divided into continuous iteroparity (primates, including humans and chimpanzees) and seasonal iteroparity (birds, dogs, etc.) Some botanists use the parallel terms monocarpy and polycarpy. (See also plietesials.)
In truly semelparous species, death after reproduction is part of an overall strategy that includes putting all available resources into maximizing reproduction, at the expense of future life (see § Trade-offs). In any iteroparous population there will, of course, be some individuals who happen to die after their first and before any second reproductive episode, but unless this is part of a syndrome of programmed death after reproduction, this would not be called "semelparity".
This distinction is also related to the difference between annual and perennial plants: An annual is a plant that completes its life cycle in a single season, and is usually semelparous. Perennials live for more than one season and are usually (but not always) iteroparous. [1]
Semelparity and iteroparity are not, strictly speaking, alternative strategies, but extremes along a continuum of possible modes of reproduction. Many organisms considered to be semelparous can, under certain conditions, separate their single bout of reproduction into two or more episodes. [2] [3]
The word "semelparity" was coined by evolutionary biologist Lamont Cole, [4] and comes from the Latin semel ('once, a single time') and pario ('to beget'). This differs from iteroparity in that iteroparous species are able to have multiple reproductive cycles and therefore can mate more than once in their lifetime. Semelparity is also known as "big bang" reproduction, since the single reproductive event of semelparous organisms is usually large as well as fatal. [5] A classic example of a semelparous organism is (most) Pacific salmon ( Oncorhynchus spp.), which live for many years in the ocean before swimming to the freshwater stream of its birth, spawning, and dying. Other semelparous animals include many insects, including some species of butterflies, cicadas, and mayflies, many arachnids, and some molluscs such as some species of squid and octopus.
Semelparity also occurs in smelt and capelin, but other than bony fish it is a very rare strategy in vertebrates. In amphibians, it is known only among some Hyla frogs including the gladiator frog; [6] [ full citation needed ] in reptiles only a few lizards such as Labord's chameleon of southwestern Madagascar, [7] Sceloporus bicanthalis of the high mountains of Mexico, [8] [ full citation needed ] and some species of Ichnotropis from dry savanna areas of Africa. [9] Among mammals, it exists only in a few didelphid and dasyurid marsupials. [10] Annual plants, including all grain crops and most domestic vegetables, are semelparous. Long-lived semelparous plants include century plant (agave), Lobelia telekii , and some species of bamboo. [11]
This form of lifestyle is consistent with r-selected strategies as many offspring are produced and there is low parental input, as one or both parents die after mating. All of the male's energy is diverting into mating and the immune system is repressed. High levels of corticosteroids are sustained over long periods of time. This triggers immune and inflammatory system failure and gastrointestinal hemorrhage, which eventually leads to death. [12]
The term iteroparity comes from the Latin itero, to repeat, and pario, to beget. An example of an iteroparous organism is a human—humans are biologically capable of having offspring many times over the course of their lives.
Iteroparous vertebrates include all birds, most reptiles, virtually all mammals, and most fish. Among invertebrates, most mollusca and many insects (for example, mosquitoes and cockroaches) are iteroparous. Most perennial plants are iteroparous.
It is a biological precept that within its lifetime an organism has a limited amount of energy/resources available to it, and must always partition it among various functions such as collecting food and finding a mate. Of relevance here is the trade-off between fecundity, growth, and survivorship in its life history strategy. These trade-offs come into play in the evolution of iteroparity and semelparity. It has been repeatedly demonstrated that semelparous species produce more offspring in their single fatal reproductive episode than do closely related iteroparous species in any one of theirs. However, the opportunity to reproduce more than once in a lifetime, and possibly with greater care for the development of offspring produced, can offset this strictly numerical benefit.
One class of models that tries to explain the differential evolution of semelparity and iteroparity examines the shape of the trade-off between offspring produced and offspring forgone. In economic terms, offspring produced is equivalent to a benefit function, while offspring forgone is comparable to a cost function. The reproductive effort of an organism—the proportion of energy that it puts into reproducing, as opposed to growth or survivorship—occurs at the point where the distance between offspring produced and offspring forgone is the greatest. [13]
In some situations, the marginal cost of offspring produced decreases over time (each additional offspring is less "expensive" than the average of all previous offspring) and the marginal cost of offspring forgone increases. In these cases, the organism only devotes a portion of its resources to reproduction and uses the rest for growth and survivorship so that it can reproduce again in the future. [14]
In other situations, the marginal cost of offspring produced increases while the marginal cost of offspring forgone decreases. When this is the case, it is favorable for the organism to reproduce a single time. The individual devotes all of its resources to that one episode of reproduction, then dies as it has not reserved enough resources to meet its own ongoing survival needs.
Empirical, quantitative support for this mathematical model is limited.
A second set of models examines the possibility that iteroparity is a hedge against unpredictable juvenile survivorship (avoiding putting all one's eggs in one basket). Again, mathematical models have not found empirical support from real-world systems. In fact, many semelparous species live in habitats characterized by high (not low) environmental unpredictability, such as deserts and early successional habitats.
The models that have the strongest support from living systems are demographic. In Lamont Cole's classic 1954 paper, he came to the conclusion that:
For an annual species, the absolute gain in intrinsic population growth which could be achieved by changing to the perennial reproductive habit would be exactly equivalent to adding one individual to the average litter size. [15]
For example, imagine two species—an iteroparous species that has annual litters averaging three offspring each, and a semelparous species that has one litter of four, and then dies. These two species have the same rate of population growth, which suggests that even a tiny fecundity advantage of one additional offspring would favor the evolution of semelparity. This is known as Cole's paradox.
In his analysis, Cole assumed that there was no mortality of individuals of the iteroparous species, even seedlings. Twenty years later, Charnov and Schaffer [16] showed that reasonable differences in adult and juvenile mortality yield much more reasonable costs of semelparity, essentially solving Cole's paradox. An even more general demographic model was produced by Young. [17]
These demographic models have been more successful than the other models when tested with real-world systems. It has been shown that semelparous species have higher expected adult mortality, making it more economical to put all reproductive effort into the first (and therefore final) reproductive episode. [18] [19]
Semelparous species of Dasyuridae are typically small and carnivorous, with the exception of the northern quoll ( Dasyurus hallucatus ), which is large. Species with this reproductive strategy include members of the genus Antechinus, Phascogale tapoatafa and Phascogale culura . The males of all three groups exhibit similar characteristics that classify them as semelparous: First, all of the males of each species disappear immediately after the mating season. Also, males that are captured and isolated from others live for 2 to 3 years. [20] If these captured males are allowed to mate, they die immediately after the mating season, like those in the wild. Their behaviour also changes drastically before and after the mating season. Before mating, males are extremely aggressive and will fight with other males if placed close together. Males that are captured before they are allowed to mate remain aggressive through the winter months. After the mating season, if allowed to mate, males become extremely lethargic and never regain their aggressiveness even if they survive to the next mating season. [20] Other changes that occur post-mating include fur degradation and testicular degeneration. During adolescence, male fur is thick and becomes dull and thin after mating, but regains its original condition if the individual manages to survive past the mating season. The fur on the scrotum completely falls off and does not grow back, even if the male survives months after the first mating season. As the marsupial ages, its testicles grow until they reach a peak size and weight at the beginning of the mating season. After the individual mates, the weight and size of the testes and scrotum decrease. They remain small and do not produce spermatozoa later in life, if maintained in a laboratory. [20] The 1966 Woolley study on Antechinus spp. noticed that males were only able to be maintained past mating in the laboratory, and no senile males were found in the wild, suggesting that all males die shortly after mating. [20]
Studies on Antechinus stuartii reveal that male mortality is highly correlated to stress and andrenocortical activity. The study measured the corticosteroid concentration in males in the wild, males injected with cortisol, males injected with saline, and females in the wild. While both males and females exhibit high levels of corticosteroid concentration in the wild, this proves fatal only to males due to females having a higher maximum high affinity corticosteroid binding capacity (MCBC). [21] Thus, free corticosteroid in the plasma of male A. stuartii rises sharply, while it remains constant in females. High levels of free corticosteroid, resulting from mating in wild males and injected cortisol in laboratory males, resulted in stomach ulcers, gastrointestinal bleeding, and liver abscesses, all of which increased mortality. These side-effects were not found in the males that were injected with saline, [21] strengthening the hypothesis that high, free corticosteroids result in higher mortality in male dasyurids. A similar study on Phascogale calura showed that similar endocrine system changes happen in P. calura as A. stuartii. [22] This supports stress-induced mortality as a characteristic of small dasyurid semelparity.
Dasyurus hallucatus, the northern quoll, is a large dasyurid and exhibits increased male mortality after the mating season. Unlike smaller dasyurids, male die-off in D. hallucatus is not due to endocrine system changes, and there was no observed spermatogenic failure after the mating season ended. [12] If male D. hallucatus survive past their first mating season, they may be able to engage in a second mating season. While the individuals in a 2001 study mostly died from vehicles or predation, researchers found evidence of physiological degradation in males, similar to the physiological degradation in small dasyurids. This includes fur loss, parasite infestations, and weight loss. As the mating period went on, males became increasingly anemic, but the anemia was not due to ulceration or gastrointestinal bleeding. [12] Lack of elevated cortisol levels during mating periods in D. hallucatus means that there is no current universal explanation for the mechanism behind increased male mortality in Dasyuridae. Post-reproductive senescence has also been proposed as an explanation. [23]
The grey slender mouse opossum exhibits a semelparous reproductive strategy in both males and females. Males disappear from their endemic area after the reproductive season (February–May). Males found months later (June–August) are of lighter body weight and the molar teeth are less worn down, suggesting these males belong to a different generation. There is a drop off in the female population, but during the months of July and August, evidence of a gap between generations like the male gap. There is also lower body weight and less molar wear observed in females found after August. This is further supported by the evidence that females that reproduce are not observed the following year. [24] [ full citation needed ] This species has been compared to a related species, Marmosa robinsoni , in order to answer what would happen if a female that has reproduced were to survive to the next mating season. M. robinsoni has a monoestrus reproductive cycle, like M. incanus, and females are no longer fertile after 17 months so it is unlikely that females that survive past the drop off in female populations would be able to reproduce a second time. [24]
Gracilinanus microtarsus , or the Brazilian gracile opossum, is considered to be partially semelparous because male mortality increases significantly after the mating season, but some males survive to mate again in the next reproductive cycle. The males also exhibit similar physiological degradation, demonstrated in Antechinus and other semelparous marsupials, such as fur loss and increase of infection from parasites. [25]
Highly elevated cortisol levels mediate the post-spawning death of semelparous Oncorhynchus Pacific salmon by causing tissue degeneration, suppressing the immune system, and impairing various homeostatic mechanisms. [26] After swimming for such a long distance, salmon expend all of their energy on reproduction. One of the key factors in salmon rapid senescence is that these fish do not feed during reproduction so body weight is extremely reduced. [27] In addition to physiological degradation, Pacific salmon become more lethargic as mating goes on, which makes some individuals more susceptible to predation because they have less energy to avoid predators. [28] This also increases mortality rates of adults post-mating.
Traditionally, semelparity was usually defined within the time-frame of a year. Critics of this criterion note that this scale is inappropriate in discussing patterns of insect reproduction because many insects breed more than once within one annual period, but generation times of less than one year. Under the traditional definition, insects are considered semelparous as a consequence of time scale rather than the distribution of reproductive effort over their adult life span. [29] In order to resolve this inconsistency, Fritz, Stamp & Halverson (1982) define semelparous insects as "insects that lay a single clutch of eggs in their lifetime and deposit them at one place are clearly semelparous or 'big bang' reproducers. Their entire reproductive effort is committed at one time and they die shortly after oviposition". [29] Semelparous insects are found in Lepidoptera, Ephemeroptera, Dermaptera, Plecoptera, Strepsiptera, Trichoptera, and Hemiptera.
Females of certain families of Lepidoptera, like the spongy moth of family Erebidae , have reduced mobility or are wingless (apterous), so they disperse in the larval stage as opposed to in the adult stage. In iteroparous insects, dispersal mainly occurs in the adult stage. All semelparous Lepidopterans share similar characteristics: larvae only feed in restricted periods of the year because of the nutritional state of their host plants (as a result, they are univoltine), initial food supply is predictably abundant, and larval host plants are abundant and adjacent. [29] Death most commonly occurs by starvation. In the case of the spongy moth, adults do not possess an active digestive system and cannot feed, but can drink moisture. Mating occurs fairly rapidly after adults emerge from their pupal form and, without a way to digest food, the adult moths die after about a week. [30]
The evolution for semelparity in both sexes has occurred many times in plants, invertebrates, and fish. It is rare in mammals because mammals have obligate maternal care due to internal fertilization and incubation of offspring and nursing young after birth, which requires high maternal survival rate after fertilization and offspring weaning. Also, female mammals have relatively low reproductive rates compared to invertebrates or fish because they invest a lot of energy in maternal care. However, male reproductive rate is much less constrained in mammals because only females bear young. A male that dies after one mating season can still produce a large number of offspring if he invests all of his energy in mating with many females. [31]
Scientists have hypothesized that natural selection has allowed semelparity to evolve in Dasyuridae and Didelphidae because of certain ecological constraints. Female mammals ancestral to these groups may have shortened their mating period to coincide with peak prey abundance. Because this window is so small, the females of these species exhibit a reproduction pattern where the estrous of all females occurs simultaneously. Selection would then favor aggressive males due to increased competition between males for access to females. Since the mating period is so short, it is more beneficial for males to expend all their energy on mating, even more so if they are unlikely to survive to the next mating season. [32]
Reproduction is costly for anadromous salmonids, because their life history requires transition from saltwater to freshwater streams, and long migrations, which can be physiologically taxing. The transition between cold oceanic water to warm freshwater and steep elevation changes in Northern Pacific rivers could explain the evolution of semelparity because it would be extremely difficult to return to the ocean. A noticeable difference between semelparous fish and iteroparous salmonids is that egg size varies between the two types of reproductive strategies. Studies show that egg size is also affected by migration and body size. Egg number, however, shows little variation between semelparous and iteroparous populations or between resident and anadromous populations for females of the same body size. [33] The current hypothesis behind this reason is that iteroparous species reduce the size of their eggs in order to improve the mother's chances of survival, since she invests less energy in gamete formation. Semelparous species do not expect to live past one mating season, so females invest a lot more energy in gamete formation resulting in large eggs. Anadromous salmonids may also have evolved semelparity to boost the nutrition density of the spawning grounds. The most productive Pacific salmon spawning grounds contain the most carcasses of spawned adults. The dead bodies of the adult salmon decompose and provide nitrogen and phosphorus for algae to grow in the nutrient-poor water. Zooplankton then feed on the algae, and newly hatched salmon feed on the zooplankton. [34]
An interesting trait has evolved in semelparous insects, especially in those that have evolved from parasitic ancestors, like in all subsocial and eusocial aculeate Hymenoptera. This is because larvae are morphologically specialized for development within a host's innards and thus are entirely helpless outside of that environment. Females would need to invest a lot of energy in protecting their eggs and hatched offspring. They do this through such behaviours as egg guarding. Mothers that actively defend offspring, for example, risk injury or death by doing so. [35] This is not beneficial in an iteroparous species because the female risks dying and not reaching her full reproductive potential by not being able to reproduce in all reproductive periods in her lifetime. Since semelparous insects only live for one reproductive cycle, they can afford to expend energy on maternal care because those offspring are her only offspring. An iteroparous insect does not need to expend energy on the eggs of one mating period because it is likely that she will mate again. There is ongoing research in maternal care in semelparous insects from lineages not descended from parasites to further understand this relationship between semelparity and maternal care.
Reproduction is the biological process by which new individual organisms – "offspring" – are produced from their "parent" or parents. There are two forms of reproduction: asexual and sexual.
The capelin or caplin is a small forage fish of the smelt family found in the North Atlantic, North Pacific and Arctic oceans. In summer, it grazes on dense swarms of plankton at the edge of the ice shelf. Larger capelin also eat a great deal of krill and other crustaceans. Among others, whales, seals, Atlantic cod, Atlantic mackerel, squid and seabirds prey on capelin, in particular during the spawning season while the capelin migrate south. Capelin spawn on sand and gravel bottoms or sandy beaches at the age of two to six years. When spawning on beaches, capelin have an extremely high post-spawning mortality rate which, for males, is close to 100%. Males reach 20 cm (8 in) in length, while females are up to 25.2 cm (10 in) long. They are olive-coloured dorsally, shading to silver on sides. Males have a translucent ridge on both sides of their bodies. The ventral aspects of the males iridesce reddish at the time of spawn.
Fecundity is defined in two ways; in human demography, it is the potential for reproduction of a recorded population as opposed to a sole organism, while in population biology, it is considered similar to fertility, the natural capability to produce offspring, measured by the number of gametes (eggs), seed set, or asexual propagules.
Reproductive success is an individual's production of offspring per breeding event or lifetime. This is not limited by the number of offspring produced by one individual, but also the reproductive success of these offspring themselves.
Internal fertilization is the union of an egg and sperm cell during sexual reproduction inside the female body. Internal fertilization, unlike its counterpart, external fertilization, brings more control to the female with reproduction. For internal fertilization to happen there needs to be a method for the male to introduce the sperm into the female's reproductive tract.
External fertilization is a mode of reproduction in which a male organism's sperm fertilizes a female organism's egg outside of the female's body. It is contrasted with internal fertilization, in which sperm are introduced via insemination and then combine with an egg inside the body of a female organism.
The yellow-footed antechinus, also known as the mardo, is a shrew-like marsupial found in Australia. One notable feature of the species is its sexual behavior. The male yellow-footed antechinus engages in such frenzied mating that its immune system becomes compromised, resulting in stress related death before it is one year old.
Antechinus is a genus of small dasyurid marsupial endemic to Australia. They resemble mice with the bristly fur of shrews.
Life history theory (LHT) is an analytical framework designed to study the diversity of life history strategies used by different organisms throughout the world, as well as the causes and results of the variation in their life cycles. It is a theory of biological evolution that seeks to explain aspects of organisms' anatomy and behavior by reference to the way that their life histories—including their reproductive development and behaviors, post-reproductive behaviors, and lifespan —have been shaped by natural selection. A life history strategy is the "age- and stage-specific patterns" and timing of events that make up an organism's life, such as birth, weaning, maturation, death, etc. These events, notably juvenile development, age of sexual maturity, first reproduction, number of offspring and level of parental investment, senescence and death, depend on the physical and ecological environment of the organism.
Phenoptosis is a conception of the self-programmed death of an organism proposed by Vladimir Skulachev in 1999.
Plant reproduction is the production of new offspring in plants, which can be accomplished by sexual or asexual reproduction. Sexual reproduction produces offspring by the fusion of gametes, resulting in offspring genetically different from either parent. Asexual reproduction produces new individuals without the fusion of gametes, resulting in clonal plants that are genetically identical to the parent plant and each other, unless mutations occur.
Cactoblastis cactorum, the cactus moth, South American cactus moth or nopal moth, is native to Argentina, Paraguay, Uruguay and southern Brazil. It is one of five species in the genus Cactoblastis that inhabit South America, where many parasitoids, predators and pathogens control the expansion of the moths' population. This species has been introduced into many areas outside its natural range, including Australia, the Caribbean, and South Africa. In some locations, it has spread uncontrollably and was consequently classified an invasive species. However, in other places such as Australia, it has gained favor for its role in the biological control of cacti from the genus Opuntia, such as prickly pear.
The dusky antechinus, also known as Swainson's antechinus or the dusky marsupial mouse, is a species of small marsupial carnivore, a member of the family Dasyuridae. It is found in Australia.
Spawn is the eggs and sperm released or deposited into water by aquatic animals. As a verb, to spawn refers to the process of freely releasing eggs and sperm into a body of water ; the physical act is known as spawning. The vast majority of aquatic and amphibious animals reproduce through spawning. These include the following groups:
The reproductive system of an organism, also known as the genital system, is the biological system made up of all the anatomical organs involved in sexual reproduction. Many non-living substances such as fluids, hormones, and pheromones are also important accessories to the reproductive system. Unlike most organ systems, the sexes of differentiated species often have significant differences. These differences allow for a combination of genetic material between two individuals, which allows for the possibility of greater genetic fitness of the offspring.
Sexual reproduction is a type of reproduction that involves a complex life cycle in which a gamete with a single set of chromosomes combines with another gamete to produce a zygote that develops into an organism composed of cells with two sets of chromosomes (diploid). This is typical in animals, though the number of chromosome sets and how that number changes in sexual reproduction varies, especially among plants, fungi, and other eukaryotes.
In behavioral ecology, polyandry is a class of mating system where one female mates with several males in a breeding season. Polyandry is often compared to the polygyny system based on the cost and benefits incurred by members of each sex. Polygyny is where one male mates with several females in a breeding season . A common example of polyandrous mating can be found in the field cricket of the invertebrate order Orthoptera. Polyandrous behavior is also prominent in many other insect species, including the red flour beetle, the adzuki bean weevil, and the species of spider Stegodyphus lineatus. Polyandry also occurs in some primates such as marmosets, mammal groups, the marsupial genus' Antechinus and bandicoots, around 1% of all bird species, such as jacanas and dunnocks, insects such as honeybees, and fish such as pipefish.
Annuality and perenniality represent major life history strategies within plant lineages. These traits can shift from one to another over both macroevolutionary and microevolutionary timescales. While perenniality and annuality are often described as discrete either-or traits, they often occur in a continuous spectrum. The complex history of switches between annual and perennial habit involve both natural and artificial causes, and studies of this fluctuation have importance to sustainable agriculture.
Biological bet hedging occurs when organisms suffer decreased fitness in their typical conditions in exchange for increased fitness in stressful conditions. Biological bet hedging was originally proposed to explain the observation of a seed bank, or a reservoir of ungerminated seeds in the soil. For example, an annual plant's fitness is maximized for that year if all of its seeds germinate. However, if a drought occurs that kills germinated plants, but not ungerminated seeds, plants with seeds remaining in the seed bank will have a fitness advantage. Therefore, it can be advantageous for plants to "hedge their bets" in case of a drought by producing some seeds that germinate immediately and other seeds that lie dormant. Other examples of biological bet hedging include female multiple mating, foraging behavior in bumble bees, nutrient storage in rhizobia, and bacterial persistence in the presence of antibiotics.
Patricia Woolley is Australian zoologist recognised for her work with marsupials, specifically the dasyurid family. Pseudantechinus woolleyae is named for her.