Adaptation of Gestation Or Egg-Laying in Species Depends on the Amount of Internal Heat Generated in Digesting the Food

Adaptation of Gestation or Egg-laying in Species Depends on the Amount of Internal Heat Generated in Digesting the Food

Karunakar Marasakatla

*Correspondence to: [email protected]

Abstract: Anatomically and physiologically, the reproductive process of gestation or egg-laying, and dietary habits in vertebrates appear to be distinct processes. An in-depth analysis of the dietary habits of vertebrates reveals that the gestation or egg-laying characteristic in these species is tightly coupled with the digestive process. Once the food has been ingested, it is then broken down to the molecular level to be absorbed into the body. The amount of energy required to digest the food depends upon the amount and composition of the food material that was ingested. The denser (ex. bones and muscle) and bigger the size of the food bits ingested, the higher the amount of energy required to break down the material - that in turn requires higher amount of gastrointestinal acids. Where there is higher amount of energy is consumed, there will be an excess amount of heat gets generated. Because of the proximity of uterus to digestive system, a layer develops around the embryo to protect it from this heat. Therefore, it appears that the higher amount of heat generated in digesting the food results in egg-laying characteristic in species such as birds and reptiles, which ingest large chunks of raw meat. Rest of the vertebrates adapted to gestation due to chewing the food into small pieces before ingesting which generates less internal heat in digestion. Species, which generate higher amount of internal heat in digestion, adapted to ectothermic nature such as reptiles. And the species, which generate less amount of internal heat, adapted to endothermic nature such as mammals. Birds are endothermic but they would have been ectothermic if there were no insulating feathers.

Key words: Dietary habits, Teeth, Chewing, Digestion, Gestation, Egg-laying, Ectotherm, Endotherm

Introduction: Vertebrates are divided between mammals and non-mammals according to the way they tend to their newborn. A common characteristic of mammals, with few exceptions, is gestation by which they grow their embryos inside the womb. Non-mammal vertebrates lay eggs. As it is evident, there are few exceptions in mammals, like platypus and echidna lay eggs. However, an in-depth analysis of the dietary habits of the vertebrates reveal that these special cases no longer appears to be special. All the vertebrates, including the special cases, fall into two distinct groups that connect the dietary habits with the adaptation of gestation or egg-laying. It appears that the species that ingest small pieces of food adapted to gestation, and the other which intake large chunks of food, comparative to body size, adapted to egg-laying.

Analysis of dietary habits: In this section, the dietary habits of vertebrates and their energy need in digesting the food after ingesting are analyzed. To categorize the dietary habits of vertebrates, a scale has been devised as shown in Table-1 based on the energy consumption in digesting a unit volume of food. Digestion is breaking down the food by gastrointestinal acids into the organic molecules for the consumption of body. For simplicity, it has been assumed that all the food ingested has been broken down into a group of organic molecules in the digestion process. The process of digestion generates internal heat proportional to the amount of energy consumed in breaking down the food, which is proportional to the amount of gastrointestinal acids generated in the stomach.

Digestion: Gastrointestinal acids + Piece of food = Group of Organic molecules + Internal Heat

PeerJ Preprints | https://doi.org/10.7287/peerj.preprints.27460v3 | CC BY 4.0 Open Access | rec: 19 Feb 2019, publ: 19 Feb 2019 It is important to note that small meal size comparative to the body generates less amount of internal heat per unit volume of the body. Similarly large meal size comparative to the body generates large amount of internal heat per unit volume of the body.

Dietary Type of food Energy Internal heat Scale requirements for generation digesting the food (Joules/m3) 1 Liquid food such as nectar and honey; Low Low Cooked food or vegetation chewed into small pieces 2 Soft invertebrates such as larvae, Low to medium Low to medium ants, termites, squid and krill 3 Whole seeds, insects, chewed raw Medium Medium meat 4 Chunks of raw meat, crushed bones Medium to high Medium to high 5 Bones and whole body consumption High High

Table-1: Dietary scale

In Table-2, the dietary habits of the birds and reptiles were analyzed. Table-3 describes the dietary habits of other vertebrates. Table-4 describes the dietary habits of the exceptional cases in vertebrates.

Species Dietary habits Dietary Gestation/ scale Egg-laying Sparrow Small insects and seeds 2-3 Egg-laying Parrot Fruit pulp with seeds and nuts 3 Egg-laying Crow Seeds, nuts and chunks of raw meat 3-4 Egg-laying Fish Whole body consumption of small fish 5 Egg-laying comparative to their body Seagull Seeds, insects and small fish 3-5 Egg-laying Eagle, Chunks of raw meat, and whole body 4-5 Egg-laying Vulture consumption of small prey Alligator Chunks of raw meat and bones 4-5 Egg-laying Snake Whole body consumption of other 5 Egg-laying vertebrates Lizard Whole body consumption of insects 5 Egg-laying

Table-2: Dietary habits of birds and reptiles

Species Dietary habits Dietary Gestation/ scale Egg laying Homo Sapiens Cooked food and vegetation chewed 1 Gestation into small pieces Cow Vegetation chewed into small pieces 1 Gestation Elephant Leaves and small branches chewed into 1 Gestation small pieces Bear Honey and ants 1-2 Gestation Lion Chewed raw meat 3 Gestation Dog Chewed raw meat 3 Gestation Hyena Chewed or chunks of raw meat and 3-4 Gestation crushed bones Dolphin Small fish and pieces of raw meat 3 Gestation Whale Krill 2 Gestation Bat Honey, fruit pulp, crushed insects 1-2 Gestation

Table-3: Dietary habits of other vertebrates.

In the absence of teeth to chew the food, birds and reptiles ingest pieces of food or whole body of the prey. As shown in Table-2, parrot and sparrow ingest whole seeds and fruit pulp or insects. Because of their small body size, the amount of internal heat generated in digesting the food per unit volume

PeerJ Preprints | https://doi.org/10.7287/peerj.preprints.27460v3 | CC BY 4.0 Open Access | rec: 19 Feb 2019, publ: 19 Feb 2019 will be large. Crow and eagle consume large pieces of raw meat, which requires large amount of gastrointestinal acids to digest the food. That in turn generates excessive amount of heat. Alligators, snakes and lizards ingest large amount of meal compared to their body size. Crocodiles have been observed to carry CO2 to digestive system to generate excess gastrointestinal acids while digesting the food [1]. As shown in Table-2, dietary scale for birds and reptiles range from three to five, at the higher end, due to the ingestion of hard to digest food. Digestion of large amount of hard to digest food generates excessive amount of internal heat that coincides with the adaptation of egg-laying in these species.

Rest of the vertebrates, with few exceptions, possesses the teeth to chew the food into small pieces before ingesting. Chewed food requires less amount of gastrointestinal acid to break down the material because of their small size. In turn, the process of digesting the food in these species generates less amount of internal heat. Small meal size and large body also reduces the amount of internal heat in digesting the food per unit volume of the body. The distance between the uterus and different digestive parts also affects the adaption of gestation or egg-laying. If the digestive parts that generate most amount of heat are away from uterus, the heat gets distributed and the impact on uterus will be less compared to when the digestive system is in the proximity of uterus. As shown in Table-3, Homo sapiens ingest cooked and chewed food, which requires less amount of gastrointestinal acid to break down the material. Cow and elephant ingests the chewed vegetation. Due to their large body size, the amount of internal heat generated in digesting the food will be less per unit volume of the body. Bat consumes the food such as honey, fruit pulp and insects. Bats appear to eat abdomen and thorax of the insects and discard the wings and legs, which were hard to digest [2]. As shown in Table-3, dietary scale for this group of species ranges from one to three, at the lower end. Possession of teeth helps to break the food apart to make it easy to digest. Therefore, it will generate less internal heat while digesting the food. Less internal heat resulted in the adaptation of gestation in these species.

Whales don’t possess teeth suitable for chewing or tearing down the food. Therefore it adapted to ingesting large amounts of krill, which is soft and easy to digest, that resulted in the adaptation of gestation in these species. Dolphins eat small fish and chunks of raw meat. Large number of teeth would have enabled the dolphin to crush the food into small pieces. Its stomach consists of three parts that facilitates the digestion in stages. The heat from the digestive parts that are away from uterus gets distributed evenly. This enables less internal heat to reach the uterus resulting in the adaptation of gestation in dolphins. Hyena appears to be an exceptional case in animals where they ingest excessive amount of crushed bones and chunks of raw meat. Does female hyenas avoid bones and chew only the meat at the time of gestation to avoid excess internal heat? It is also possible that their tolerance of internal heat is higher than other animals to support the gestation. In general, less amount of internal heat in this group of vertebrates due to the ingestion of soft or chewed food resulted in the adaptation of gestation.

Species Dietary habits Dietary Gestation/ scale Egg-laying Echidna Whole body consumption of small 5 Egg-laying vertebrates Platypus Whole body consumption of small 5 Egg-laying vertebrates

Table-4: Dietary habits of the exceptional cases in vertebrates.

The general rule was that the placentals were considered as mammals and monotremes were considered as non-mammals. As shown in Table-4, some of the vertebrates didn’t exactly fall under the general definition of mammals or non-mammals. Echidna and platypus were defined as mammals but anatomically they were monotremes. These two species ingest whole body of insects in the absence of teeth. Digesting large amount of insects generate excessive internal heat comparative to their body size. Therefore these two exceptional cases in mammals adapted to egg-laying. Their dietary scale lies at the extreme higher end.

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Hypothesis: Amount of energy consumed in digesting the food depends upon whether it is vegetation or meat, and how finely the food is chopped or chewed before consuming. Once the food is in the digestive tract, the amount of energy required to digest pieces of meat will be more than chewed vegetable products. At the same time, the amount of energy required would be more in digesting the whole animal compared to chopped or chewed pieces of meat. In the process, body generates the gastrointestinal acids in proportion to the meal size and strength and size of the food bits. Gastrointestinal acids break the food material to organic molecular level for consumption. A byproduct of energy usage is generation of internal heat. As more and more energy is required to digest the food, more heat will be generated inside the body. It is important to note that the heat generated in chewing the food material doesn’t add to the internal heat, instead it dissipates at head. Because of the proximity of uterus to digestive tract, the heat generated in digesting the food will have an effect on the embryonic development. Species, which consume chunks of meat and whole body of prey, will generate more heat in digesting the food. As a result, these species adapted to egg- laying in the reproductive process to protect the embryo from the excessive internal heat. Species that ingest finely chopped or chewed food with small meal size requires less energy in digesting the food. In turn there will be less internal heat gets generated. These species adapted to gestation because of the conducive environment for prolonged nourishing of the embryo inside the womb. Additionally, the species, which generate higher amount of heat in digesting the food, turned out to be ectothermic and the other, which generates less internal heat, became endothermic.

Discussion: After grazing the grass, cows spend lot of energy in chewing the regurgitated food to avoid excessive amount of gastrointestinal acid required to digest the food, therefore avoiding additional amount of internal heat. Heat generated in chewing the food gets dissipated at the head and doesn’t add up to the internal heat. Molar teeth appear to be essential for species to adapt gestation. Molar teeth help in grinding the food into small pieces before entering into the digestive system.

In absence of molar teeth, whales adapted to eating soft material (krill) resulting in the gestation. Even though aardvarks have molar teeth, they were not efficient in chewing the food, therefore it adapted to eating only ants and termites, which were easy to chew before ingesting. This resulted in gestation in aardvark. Echidna has similar diet to aardvark but in the absence of molar teeth, echidna crushes the ants and termites before ingesting. Crushing is not as efficient as chewing to break down the food. This resulted in the adaption of egg-laying in echidna. Giant anteater has no teeth. Therefore it adapted to eating ants and termites similar to echidna. But it adapted to gestation instead of egg- laying. The giant anteater uses the formic acid of the prey to digest the food, which results in less internal heat compared to using gastrointestinal acids. This resulted in the adaptation of gestation in giant anteaters. Similar to giant anteaters, pangolins lack molar teeth and feed mostly on ants and termites. Its stomach contains inward pointing spines that enable crushing the food for efficient digestion. This enabled the pangolins to adapt gestation in the reproduction process.

Efficiency in melting the medullary bone to form the shell around the embryo in egg-laying species is possibly dependent on the amount of internal heat generated from digesting the food. Hard to digest food such as chunks of raw meat, insects, and nuts and seeds require more gastrointestinal acid to digest than the soft material, which in turn generate more internal heat. Higher efficiency in melting the medullary bone is possibly due to the higher amount of internal heat. A change in diet towards softer material possibly results in the lesser efficiency in melting the medullary bone.

It is possible that the duration of gestation also depend on the type of food and the time it takes to digest. Soft food may result in prolonged gestation and hard to digest food might result in short gestation period. As the difficulty in digesting the food increases, species adopted to shortened gestation in the form of egg-laying. Giant panda adapted to consume hard to digest bamboo. The excess internal heat in digesting the bamboo reduced its gestation period compared to a mammal of similar size. This resulted in the smallest newborn compared to the size of the mother. Similar to

PeerJ Preprints | https://doi.org/10.7287/peerj.preprints.27460v3 | CC BY 4.0 Open Access | rec: 19 Feb 2019, publ: 19 Feb 2019 pandas, marsupials dietary habit include hard to digest food with shortened gestation period of few weeks. Wombat digestion takes around eight to 14 days and the gestation period is around 20 days. Therefore marsupials fall in the middle of egg-laying (reptiles) and longer gestation period (placentals), where they generate medium internal heat in digesting the food.

In general, egg-laying mammals, marsupials and placentals were observed in the increasing levels of body temperature with some exceptions [3,4]. Echidna and platypus generate excess amount of heat in digesting the food. These species adapted to lower body temperatures to absorb the excess heat generated in digesting the food. By adapting to lower body temperature, these animals avoided internal overheating during digestion. Similarly, marsupials adapted to medium body temperature to absorb the medium levels of heat generated in digesting the food. Whereas placentals adapted to higher body temperature because of less internal heat generated in digesting the food. Therefore the dietary habits of mammals resulted in the adaptation of endothermic nature. All the birds generate excess amount of heat in digesting the food due to their dietary habits. Because of the insulating feathers, heat would have trapped inside the body becoming the endothermic species. Body temperature of the birds is higher than mammals. Reptiles generate excess amount of heat in digesting the food. In the absence of insulating feathers, these species would have adapted to ectothermic in nature.

Different species of sharks have been observed to exhibit various reproduction methods such as ovoviviparity, oviparity, and viviparity. Ovoviviparity is where the embryo in yolk sac hatches in the oviduct of the mother. Oviparity is where they lay the fertilized eggs in the water. Viviparity is where gestation occurs without using the yolk sac. Sharks posses teeth but they are not suited to break the food into small pieces. Therefore, they ingest small fish and large pieces of raw meat and bones. After digestion in initial chamber, they let through the soft material into rest of the digestive tract and discard rest of the material by vomiting. This reduces the need to digest hard materials such as bones. Sharks also vary in size from small to large with varying differences in the type of food they ingest. Body size and meal size variances might generate different levels of internal heat. This resulted in some species of sharks adapting to gestation and the other to egg-laying depending on the internal heat generated while digesting the food. Different species of frogs have also been observed to lay eggs or give birth to tadpoles [5]. Different species of salamanders also adapted to different reproductive processes. It is possible that the dietary habits forced the adaptation of gestation or egg-laying characteristic in these species.

Fish also exhibit adaptation to different reproductive processes. Diet of guppies and mollies include algae, aquatic invertebrates and aquatic insect larvae. All of these food materials are easy to digest which resulted in the adaptation of gestation in these particular species. Most of the insects are egg- laying species, however scorpions adapted ovoviviparity. Scorpions shred its prey into pieces using its claws and inject gastrointestinal acids into its prey. Then it intakes the resulting liquid food and discards rest of the hard material from its prey. By ingesting externally digested liquid food, it basically avoided the generation of excess internal heat, which helped it to adapt gestation.

Further exploration The analysis presented in this article suggests that the difficulty in digesting the food determines the adaption of egg-laying or gestation in species. If the hypothesis presented in this article turned out to be true, it will pave the way for further study on the affect of internal heat in embryonic development and other physiological processes in the following areas. a) Nutrition of the food alone can’t explain the functionality of the body. Nutrition along with the strength of the material and how long it takes to digest will have impact on the functionality of the body. In an earlier study, eating nuts were observed to reduce major chronic diseases [6]. Chewing nuts consumes energy and digesting dense bits of nuts requires more gastrointestinal acids, which will contribute to the internal heat. It is possible that these factors would have enabled the reduction in the chronic diseases when nuts were part of the regular diet.

PeerJ Preprints | https://doi.org/10.7287/peerj.preprints.27460v3 | CC BY 4.0 Open Access | rec: 19 Feb 2019, publ: 19 Feb 2019 b) Mammal like chewing has been observed in some species of dinosaurs [7]. Are these species adapted to gestation instead of egg-laying as widely believed? c) Dogs have been observed to eat less in the first two weeks of pregnancy. This will reduce the internal heat due to reduced use of gastrointestinal acids. Are there any other species that exhibit change in behavior during the pregnancy? d) Is the shortened gestation period or premature birth in humans related to the abnormal internal heat generated due to the ingestion of hard to digest food similar to panda and marsupials? e) Ancestral panda is thought to be carnivorous or omnivorous [8]. Stable isotope analysis of ancient panda bone and tooth samples suggests that they possibly had more complex diet [9]. Does ancient panda had longer gestation period if the diet contained easy to digest food? f) Once a species has been adapted to a specific diet and body temperature, continuation of that species depends on the availability of regular diet. Any changes in diet will have a variance in the body temperature, which affects the gestation process. It is possible for a species to go extinct if there is a drastic change in dietary habits.

Conclusion Even though the vertebrates were divided based on how they tend to their young ones after the birth, it is also possible to divide the vertebrates based on their dietary habits. Analysis of dietary habits of vertebrates strongly suggests that these habits force the species to adapt egg-laying or gestation based on the internal heat generated while digesting a single meal. Birds and reptiles along with echidna and platypus adapted to egg-laying because of high amount internal heat generated while digesting the food. Rest of the vertebrates adapted to gestation because of less amount of heat generated while digesting the food. Therefore, the type and availability of food resource along with meal size and how finely food is broken down before ingesting are tightly coupled with reproductive process of egg-laying or gestation in the animal kingdom. Species, which ingest large meal comparative to their body, appear to transform into ectothermic and the species that ingest small meal size appear to become endothermic. You are what and how you eat.

Acknowledgements Author would like to thank Soumya Marasakatla for critical comments, discussion and editing the earlier versions of the document.

This work is dedicated to all mothers - vertebrate or invertebrate, adapted to gestation or egg-laying.

Declaration of interests Author declares no competing interests.

Funding Author self funded the work.

Preprint version 1 of the article was published on 31 December 2018.

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PeerJ Preprints | https://doi.org/10.7287/peerj.preprints.27460v3 | CC BY 4.0 Open Access | rec: 19 Feb 2019, publ: 19 Feb 2019 5. DT Iskandar, BJ Evans, JA McGuire, (2014) A Novel Reproductive Mode in Frogs: A New Species of Fanged Frog with Internal Fertilization and Birth of Tadpoles. PLoS ONE 9(12): e115884. https://doi.org/10.1371/journal.pone.0115884 6. Y Bao, J Han, FB Hu, et al, (2013) Association of nut consumption with total and cause- specific mortality. N Engl J Med 369(21): 2001-2011. 7. FJ Varriale, (2016) Dental microwear reveals mammal-like chewing in the neoceratopsian dinosaur Leptoceratops gracilis. PeerJ 4:e2132; https://doi.org/10.7717/peerj.2132 8. Q Zhanxiang, Q Guoqin, (1989) Ailuropoda found from the late Miocene deposits in Lufeng, Yunnan. Verteb. Palasiat. 27 (153-169). 9. H Han, W Wei, et al, (2019) Diet evolution and habitat contraction of giant pandas via stable isotope analysis. Current Biology 29 (1-6). https://doi.org/10.1016/j.cub.2018.12.051

Notes A. Anatomical structures, dietary habits and reproductive characteristics of the species listed in this article were gathered from online resources such as Wikipedia.org and Arkive.org.

PeerJ Preprints | https://doi.org/10.7287/peerj.preprints.27460v3 | CC BY 4.0 Open Access | rec: 19 Feb 2019, publ: 19 Feb 2019