Animal as a source and inducer of
Animal development is regulated by biotic and abiotic factors. In this work we intend to focus on the environment as a source and inducer of genotypic and phenotypic variation and as an evolutionary agent. Thus, in this work we will talk about the concept of ecological evolutionary developmental biology, most commonly known as Eco-Evo-Devo. This field aims to uncover how the environment interacts with an organism’s genome and development (Landry and Aubin-Horth, 2014; Gilbert, Bosch and Ledón-Rettig, 2015). This term is a fusion of the already existing evolutionary developmental biology (Evo-Devo) with ecology, including other known developmental concepts, such as developmental plasticity, developmental symbiosis, polyphenisms, epigenetics, among others (Abouheif et al., 2014; Gilbert, Bosch and Ledón-Rettig, 2015).
In fact, it is no longer reasonable to consider animals purely as individuals, without taking into account their symbiotic interactions with other organisms. Symbiotic interactions are fundamental for animal development. Anatomical and physiological criteria is no longer enough, since symbiosis provides the organisms with a unique mode of genetic inheritance. As Gilbert said, “No organism evolves alone” (Gilbert, 2012).Organisms in their embryonic or larval stages can respond to environmental variations, changing their morphology, physiology and behaviour. This ability is called developmental plasticity, and it is in the origin of new traits that may cause organisms to change their form, physiology, or behaviour (West-Eberhard, 2005; Gilbert, Bosch and Ledón-Rettig, 2015), and potentially improve their viability under certain environmental conditions.
This is the first process that leads to species differences under natural selection (West-Eberhard, 2005). The necessary reorganization of the phenotype, to produce new variants upon environmental or genomic stimuli is achieved through developmental recombination of the ancestral phenotype (West-Eberhard, 2003). New developmental variants, in the form of the regulation or formation of a new trait, establish themselves in populations and species due to genetic evolution, through selection of phenotypes, when there is a genetic component.According to West-Eberhard, developmental effect of new variations, like genomic mutations, or changes caused by the environment, such as a pathogen or a climate shift, only occurs if the pre-existing phenotype is responsive to it. So, without developmental plasticity, the bare genes and environmental demands would not cause any response on the phenotype, nor would they present an evolutive importance (West-Eberhard, 2005). Another important process is developmental recombination, which occurs upon a new input. This input causes a reorganization of the phenotype, providing new material for natural selection to work on (West-Eberhard, 2005). The third and final process that contributes to intra-species variability is genetic accommodation.
If the acquired phenotypic variations are heritable, in other words, when there is a genetic component, natural selection favors those alleles or allele combinations that have a fitness effect and allow the expression of the new trait. These new traits may, subsequently, be genetically assimilated into the lineage, and might even prosper, as a consequence of environmental changes, to the detriment of the preexisting characters (West-Eberhard, 2003; Gilbert, Bosch and Ledón-Rettig, 2015). In this way developmental plasticity are considered as a major force in adaptation, speciation and macroevolutionary change (Gilbert, Bosch and Ledón-Rettig, 2015).The concept of phenotypic plasticity is also important to understand Eco-Evo-Devo, and it should not be confused with developmental plasticity. Phenotypic plasticity represents the basis of the relationship between phenotypic variation and environmental influence on the development, that may eventually be mediated by natural selection.
This plasticity includes environmental action on several stages of development, contrarily to developmental plasticity which refers to early phase only (Oliveira et al., 2016). Phenotypic plasticity can be divided in two main types: polyphenism and the reaction norm (Gilbert, 2000). Polyphenism occurs when two or more distinct phenotypes originate from the same genotype, based on environmental cues, such as the climate, or population density (Gilbert, 2000; Simpson, Sword and Lo, 2017). One example is the polyphenisms of the butterfly Araschnia levana that present different forms if the butterflies eclose in the spring or in summer; the spring morph is bright orange with black spots, while the summer form is mostly black with a white band (Gilbert, 2005). About the reaction norm, this term refers to the spectrum of potential phenotypes expressed by a genotype in different environmental conditions (Stearns, de Jong and Newman, 2017) – the most adaptive phenotype is selected by the environment, within genetically-determined limits specific to the gene itself (Gilbert, 2000). An example it is the study referred in (Gilbert, 2001) with wood frog, Rana sylvatica, that in presence of predatory larval dragonfly Anax grow smaller than those without predators. This is a reaction norm that depend of the number and type of predators.
The addition of more predators leads to a continuously deeper tail fin and tail musculatureUnder the optics of phenotypic plasticity, new phenotypes could emerge from reaction norms present in the genetic variation already existing in the population, without necessarily have a new allele with phenotypic effects (Oliveira et al., 2016).Eco-Evo-Devo can also be combined with ecological genomics, for the investigation of development in its ecological context. This merge will increase the current knowledge of evolution, and of the genetic and regulatory mechanisms behind the expression of traits important to function, fitness, and ecological interactions in their environment (Abouheif et al., 2014).Amphibians as an eco-evo-devo model For many decades, amphibians have been used as study models to assess the sensitivity of vertebrates to environmental variations, since they are highly responsive to a wide variety of environmental factors. In this context, we intend to refer to amphibians as a model to explain the Eco-Evo-Devo concept. Firstly, we will explain how the normal development of these organisms occurs, and, posteriorly, we will illustrate how certain environmental factors can influence this process.
The life cycle of an organism is a standardized pattern, which consists of three events that mark the passage of one generation to the next – physiological, genetic, and morphological. Further, there are two other important points, which are the birth and death of the individual (Andrews, 2017).There are two types of life cycles (Andrews, 2017): The complex life cycle (CLC): It is described by zoologists as “an abrupt ontogenetic change in an individual’s morphology, physiology, and behaviour, usually associated with a change in habitat”. An organism that passes through two or more such (irreversible) distinct phases is considered to have a CLC. A classic example is the frog, in which some species occupy two distinct ecological niches and lifestyles: an aquatic herbivore in the tadpole phase, and a terrestrial carnivore in the adult stage.The simple life cycle (SLC): Occurs when the offspring of a species are born into the same habitat occupied by the adults, and do not undergo sudden morphological or ontogenetic changes. Some examples include birds, humans, and other mammals. In this section, we will consider the example of Spadefoot toads (Pelobates syriacus) from Israel, to explain the development of this species (life cycle) and which factors can influence its normal development.
As previously mentioned, frogs have a CLC, and so has Pelobates syriacus. This means that during the life cycle (Figure 1) of this species, it required two places for living. The breeding places consists in terrestrial habitats, such as sandy soils, heath lands and deciduous woodlands with loamy soils, while the spawning biotopes include a variety of permanent or semipermanent ponds (Degani, 2015).During the breeding season, males are the first to arrive at the pond, sending out a mating call. This call consists of a short, explosive “wonk”. Afterwards, the females arrive, and breeding occurs underwater. The amplexus happen when the male holds the female above the back legs. While they swim together (still in the amplexus position), the female releases the eggs.
This species can breed several times during the warm season, and in the darkness of night (Degani, 2015).The distribution, habitat, and selection of breeding place are influenced by several aspects, such as water availability during the spring and early summer, larval growth and complete metamorphosis, burrowing behaviour, physiology adaptations to various environments, and the species’ biology (Degani, 2015).The larval period of Pelobates syriacus can last several months until metamorphosis. to Degani (2015), the breeding places selection is correlated with the abundance of water in the pond (it should be available for few months), and water temperature (must be above 20°C and most of the time above 25°C), because of the long periods needed to complete metamorphosis.Another unique characteristic of this species is that spends 8- 10 months of the year buried in the soil. During the summer, the soil dries out, and the osmotic relationship between the toad and the surrounding soil changes. At a certain point, water begins to pass from the toad to the soil (or the air) and the toad becomes dehydrated. This burrowing behaviour of metamorphosed Spadefoot toads is a very important physiological adaptation to terrestrial life, because of the accumulation of urea and electrolytes in the plasma (Degani, 2015).
The life cycles of the amphibians can be interrupted by numerous causes that lead to their decline, nominated habitat destruction, exotic predators, pollution and utilization as food and pets as possible causes. Besides, three more potential causes were added to the list: effects of climate change, disease in combination with environmental factors, and increased levels of ultraviolet radiation (Sparling et al., 2010). Ecological influence in developmentIn order to explain how ecological changes can influence amphibian’s development and results in phenotypic variations, and how natural selection intervene to fix this variation, we consider in this section a study carried out by Kaplan and Phillips (2006) in Bombina orientalis.
The objective of this study was to analyse variations in Bombina orientalis development from two approaches: effects on temperature and effects at the maternal level, egg size, but it will considered only the temperature effects in this work because the maternal effects did not show a significant influence in the study. The data collected for this study refers to the years 1993 and 2000.In a first phase of the study, the temperature variations and incubation time variation in the two years under study were registered. The hottest lake where the eggs were deposited was at an average temperature of 22.4 °C in 1993 and 23.4 °C in 2000.
The incubation time showed to be very variable, between 2.2 and 8.6 days. All obtained data were then associated, and it was found that at higher temperatures the incubation time is lower, contrary to what happens at lower temperatures where the incubation time is longer. Concerning to morphological analyses, corneal transparency was used to define the differentiation stage at the time of incubation, and it was verified that it occurred in stage 19 and 21. Based on the observations, the authors demonstrated that higher temperatures have negative effects on the truncation of the incubation period, consequently decreasing both length and height of the tail, however, it has a positive effect on the dimensions from the snout to the posterior margin of the vent. Contrarily, at lower temperatures, the incubation time is longer, resulting in increase in both length and height of the tail, and decrease of the length from the snout to the posterior margin of the vent.In terms of performance, tail size has a positive influence on performance in terms of speed.
By contrast, the larger the length from the snout to the posterior margin of the vent, the slower it swims. Performance is intimately associated with the survival rate, resulting in better chances of survival. So, organisms that develop in lower temperatures have better chances to survive compared to those which develop in higher temperatures.However, several other environmental factors may influence animal development, including abiotic factors, such as food and water availability, and biotic factors, like the presence of predators or crowding. Althout it has to be noted that these factors do not always have fitness effects.
An example of this is the case of predator-induced polyphenism, in which, in the presence of snakes, the embryos of Agalychnis callidryas vigorously shake in their egg cases. In seconds, they hatch prematurely into the water and embryos that don’t hatch quickly are eaten. This type of polyphenism, induced by predator, is considered a trade-off, because once in the water, these premature forms are at higher risk for being eaten by the aquatic predators (Gilbert, 2001).ConclusionsOrganisms with a complex life cycle occupy different niches during their life, as is the case of amphibians.
These niche variations are associated with alterations of environment that can induce morphological, physiological and behaviour changes. In this work, we used amphibians as a model to explain the Eco-Evo-Devo concept. The life cycle of these organisms consists in 6 phases,and the environmental variations can induce alterations mainly in early phases. Several environmental variations are known as inducers of new phenotypes, including abiotic factors, such as temperature, food availability and salinity, and biotic factors, such as the presence of predators or crowding, or even stress situations. The induced emergence of new phenotypes can have a genetic component and natural selection acts to favor the most apt phenotype.To conclude, with this work we intended to demonstrate that environments have an intimate relationship with the organism’s development, which result in variations that can be a key of evolution of some organisms, because nature can act as a inducer and a regulator, allowing the emergence and survival of new phenotypes.