Overview

Niche construction arises in development: it occurs through the activities of individual organisms during their lifetime (ontogeny) as they modify environmental states, and has ecological and evolutionary consequences when those individual-based local effects scale up across populations, and over time. By modifying their local environment, organisms can affect their own future development, whilst the construction of nests and other ‘nursery’ environments can shape and regulate the conditions experienced by developing offspring. For these reasons, niche construction theory is explicit about the need to treat niche construction as both a developmental process and a cause of evolution (Odling-Smee et al. 2003).

There exists a complementarity between the fields of niche construction and ecological developmental biology (Laland et al. 2008). Niche construction emphasizes the ability of the organism to modify the environment to form a supportive niche, whilst ecological developmental biology emphasizes the ability of environmental agents (e.g. temperature, density, symbionts) to modify the developing organism.

Animal and plant development provide some of the most direct examples of niche construction (Gilbert 2020). Here, two modes of niche construction can occur, often simultaneously. First, the developing organism can modify its environment to construct niches for its own development. Second, the organism can become the niche for other organisms that will later alter it. Both of these modes involve developmental plasticity–the ability of an organism to change its phenotype in response to the presence of environmental agents.

Developing organisms modify their own environments to construct niches

The formation of galls by gall wasps and the formation of the placenta by mammalian embryos are examples of how organisms construct their own developmental environment. The female goldenrod gallfly lays its eggs on the goldenrod. When they hatch, the caterpillars eat the goldenrod stem, and their salivary proteins induce cell proliferation in the goldenrod, triggering formation of a gall. The larva enters the gall, which becomes its home, and continues eating from within. As winter approaches, the larva begins to produce sugars that act as an antifreeze. The trigger for this synthesis is not temperature but aromatic substances produced by the desiccating gall (Williams & Lee, 2005). Here, we see both reciprocal induction on ecological level and reciprocal causation at evolutionary level. The gallfly larva creates a niche by causing the plant to change its development, and that niche provides safety, nutrition, and the cue for the larva to change its development as winter approaches.

Mammalian development provides another example. Mammalian embryos construct their niche by instructing the uterus to alter its cell cycles, its adhesion proteins, and by inducing the formation of blood vessels. The fetus induces changes in the uterus preparing it for implantation of an embryo, thereby causing the uterus to become a habitat for the developing organism. In return, the uterus reciprocally helps induce the formation of the placental tissues of the embryo (Spencer et al. 2004; Ticconi et al. 2006).

Niche construction during development can also be the product of behavior. For instance, female dung beetles manufacture and bury a brood ball of dung and insert into it a faecal pedestal onto which they lay an egg. Through this niche construction they provide a safe home, food supply and microbiome for their developing young (Schwab et al. 2016). The developing larvae also engages in niche construction, in a manner that affects its development. It processes the brood ball in ways that propagate and change the composition of the microbiome. Experiments show that both maternal and offspring niche construction strongly affect offspring size, fitness and trait characteristics, such as sexual dimorphism (Schwab et al. 2016, 2017). This example illustrates how niche construction can both shape developmental trajectories and affect evolutionary outcomes. Ongoing work is exploring how beetle populations diverge in their reliance on certain forms of niche construction, and how it affects range expansions and reproductive isolation.

Organisms construct their environment and alter each other

One of the most exciting areas of developmental niche construction concerns symbiotic bacteria. Here, the bacteria are both part of the environment and an organism seeking a niche. Bacteria and developing animal are environments for each other, and scaffold each other’s development (Chiu and Gilbert 2015). Bacteria are an essential component of the inheritance system in many insects and vertebrates. For instance, Dedeine et al. (2001) found that females of the wasp Asobara tabida cannot make their oocytes without products being made from the Wolbachia bacteria stored in them: A. tabida treated with antibiotics were unable to produce mature eggs.

Similarly, mammalian development is not complete without signals from symbiotic bacteria (Hooper et al. 2001; Xu and Gordon 2003). Mice bred without gut bacteria have aberrant digestive systems and defective immune systems. The bacteria induce gene expression in intestinal epithelia, and these genes are responsible for activating the pathways that allow intestinal capillaries to form and lipids to be transported (Hooper et al. 2001; Stappenbeck et al. 2002). Without these microbes, mice lack the capillary vasculature of the intestinal villi.

Ley et al. (2006) have shown that human babies acquire their gut microbial communities from the vagina and the feces of their mothers early in life. Babies born through Caesarian section had an altered colonization pattern compared with vaginally delivered babies.

Niche construction by symbionts has been studied extensively in the squid Euprymna scolopes and the luminescent bacterium Vibrio fischeri (McFall‐Ngai & Ruby, 1991; Montgomery & McFall‐Ngai, 1994). The adult squid is equipped with a light organ composed of sacs filled with light‐emitting bacteria, but newly hatched squid have neither the bacteria, nor the light organ to house them. Rather, the symbiotic bacteria interact with the larval squid to build their niche. The juvenile squid acquires the bacteria from seawater by pumping through its mantle cavity (Nyholm et al. 2000). The bacteria bind to a ciliated epithelium in this cavity, and secrete chemicals that induce hundreds of genes in the epithelium to become active, leading to the differentiation of the surrounding cells into storage sacs for the bacteria, and the expression of genes encoding opsins and other visual proteins in the light organ (Chun et al. 2008; Koropatnick et al. 2004; McFall‐Ngai. 2008; Tong et al. 2009). In this mutualistic arrangement, both organisms change their gene expression patterns, in a beneficial way. The bacteria get a niche, and the squid develops a light organ that allows it to swim at night.

Another interesting case of bacterial niche construction concerns the formation of the rumen of ruminants such as cattle, sheep and deer. Newborn calves have sterile rumens, and the digestive tube becomes colonized by microbes as the calf pass through the birth canal. When the calf starts eating solid food, bacteria produce plant-wall‐digesting enzymes that metabolize the polysaccharides. Over 70% of the cow’s energy comes from this microbial digestion of plant fiber (La Reau & Suen, 2018). The bacteria in the rumen multiply when given this food, and as they proliferate, they produce volatile fatty acids, that cause the rumen to grow and complexify (Gilbert, 2020). Here, the gut bacteria help construct their niche, the rumen, without which the cattle could not survive.

Many experiments now show that symbionts are not merely passive travelers, but provide essential functions for their hosts. In mammals, it has been estimated that 50-90% of cells are symbionts (Bäckhed et al. 2005; Sender et al. 2016). For instance, about one-third of the metabolites in our blood are derived from bacteria, whilst symbionts have been shown to be critical for normal brain development, and effective functioning of the immune system (Gilbert & Epel 2009; Gilbert et al. 2012). The bacteria of the gut are critical in the organogenesis of the gut capillaries and lymphoid tissues (Round et al. 2010). 

Microbiomes (symbionts such as bacteria, archaea, protists, fungi and viruses) can be transmitted from one generation to the next, including via eggs and seeds, through the birth canal in mammals, or by drinking mother’s milk (Gilbert et al. 2012; Roughgarden et al. 2018). Many organisms rely on their microbiome to carry out essential processes: for example, corals rely on microalgae for photosynthesis and energy production, termites rely on intestinal protists to digest cellulose, and legumes require rhizobial bacteria for nitrogen fixation (Kamra 2005; Gilbert et al. 2012; Roughgarden et al. 2018).

“Development is a multi-species project” (Chiu & Gilbert 2015), and microbial communities do not merely “occupy” hosts but rather host and microbiome “are constantly constructing and modifying each other as local niches” (Chiu & Gilbert 2015).

Extra-genetic inheritance and the ‘start-up niche’

The inheritance of symbionts from the mother is an example of extra-genetic inheritance. Recent years have witnessed the accumulation of empirical support for extra-genetic inheritance through multiple pathways, including epigenetic, ecological, behavioral, and cultural inheritance systems and the transmitted microbiome (Bird 2002; Jablonka & Lamb 2005; Bonduriansky & Day 2018). Diverse resources are transmitted from parents to offspring, including components of the egg, hormones, symbionts, epigenetic marks, prions, small RNAs, antibodies, ecological resources and learned knowledge.

Traditionally considered proximate causes of development, it is now evident that some of these factors can lead to the inheritance of phenotypes, and many researchers now attempt to integrate these components into an extended concept of heredity (Bonduriansky & Day 2018; Danchin et al. 2011; Jablonka & Lamb 2014). These additional pathways allow for ‘soft’ inheritance (environmental influences on heredity). Recognition of extra-genetic inheritance has important implications, both for understanding development and comprehending how development can influence evolution.

Offspring inherit not just genes but a ‘start-up niche’, comprising a specific parentally chosen location for birth and a transmitted package of resources (Odling-Smee 2010). For example, phytophagous insects typically choose to lay eggs on specific host plants, which become food for their larvae, whilst in birds, nutrients and hormones are provided in the yolk for embryonic nutrition. Many organisms provide protective chemicals for their offspring in this start-up niche, including antibodies such that the young can survive before their immune systems mature (birds, mammals), compounds that are poisonous or distasteful to predators (moths) (Dussourd et al. 1988), or even sun-blocks that protect transparent embryos and larvae from the effects of solar radiation (Goldstone et al. 2006).

From the niche-construction perspective, the key task for any developing organism becomes the active regulation of its inherited ‘niche’, by responding to its environment, and by altering its environment, in ways that keep its personal organism–environment relationship continuously adaptive, for the rest of its life. This active ‘niche regulation’ undermines the (generally assumed) independence of environments from developing organisms: just like selective environments, developmental environments are not independent on the organism. Niche construction provides a pathway through which developmental processes can influence evolutionary processes.

Many researchers have argued that development plays significant, but not yet fully appreciated, evolutionary roles (e.g. Gould & Lewontin 1979; West-Eberhard 2003). For instance, micro- and macro-evolutionary patterns are commonly viewed as shaped by developmental biases and constraints (Jablonski 2020; Jackson 2020), while developmental plasticity is perceived to provide phenotypic variants that can be later stabilized by the natural selection of genetic variation (Gilbert et al. 2015; Uller et al. 2020; Levis & Pfennig 2020). Genes can be ‘followers, not leaders’ in evolution (West-Eberhard 2003). Niche construction contributes to these mechanisms (Laland et al. 2008; Hall 2012; Chiu & Gilbert 2015; Roughgarden et al. 2018).