Segmentation is a combination of multiple developmental processes that span from the first expression of segmentation genes to the complete display of all the morphological features of a mature segmental body unit. Since segmental units undergo developmental patterning (which may involve size, shape, limb formation, etc.), the “segmental stage” at which a segment can be considered “laid down” is an arbitrary choice. For instance, in the anostracan crustacean Artemia, this was identified either with the “segmental stage c,” at which the segment has the shape of a short cylinder (Weisz, 1946), or with the appearance of a stripe of Engrailed protein at the prospective posterior boundary of the segment (Williams et al., 2012).

For our comparative purposes, we count as developmental addition of a new segment the first morphological appearance of a segmental unit as traditionally recognized by descriptive morphology (not necessarily the same for all taxa), irrespective of how close it is to its final morphology (e.g., disregarding presence/absence of limb buds). We calculated a degree of anamorphosis as the percentage of segments that are added during post-embryonic life, from 0% in epimorphic taxa, to >95% in the longest millipedes (see Supplementary Table 1 for details on segment count).

Independent from the degree of anamorphosis, three main modes of anamorphosis are recognized, as first proposed by Enghoff et al. (1993) for millipedes. In euanamorphosis, segment number increases at each molt throughout the whole post-embryonic life, to terminate only with the death of the animal. In teloanamorphosis, segment number also increases throughout the animal's life, but both the number of molts and the schedule of segment addition at each molt are fixed for a given species and sex. Finally, in hemianamorphosis, the post-embryonic development includes a first anamorphic phase, through a first batch of stages (instars) separated by molts, followed by an epimorphic phase where molts take place without further increase in the number of body segments.

The distribution of anamorphosis and epimorphosis in the main groups is shown in Figure 1 (reference to source data in Supplementary Table 1).

In Chelicerata, hemianamorphosis is found among the Pycnogonida, which are sister to all the other Chelicerata, the Euchelicerata; these are all epimorphic to the exclusion of the Acariformes. Within the Pycnogonida and Acariformes, a few lineages have independently evolved epimorphic development (Lindquist, 1984; Brenneis and Arango, 2019).

Most myriapod lineages are hemianamorphic. Epimorphic development only occurs in the centipede clade rightly named Epimorpha, which includes the Scolopendromorpha and Geophilomorpha. Euanamorphosis and teloanamorphosis are found among the Helminthomorpha millipedes exclusively, where both modes may have evolved once or several times independently (Miyazawa et al., 2014).

Within the Pancrustacea, hemianamorphosis is the most common developmental mode among the “crustacean” (non-Hexapoda) lineages, but epimorphic development has evolved in some lineages, in association with direct development, whereas teloanamorphosis has possibly evolved in Copepoda (Huys, 2014) and euanamorphosis in Remipedia (Koenemann et al., 2009). Within the Hexapoda, only the Protura are hemianamorphic, while the Collembola, Diplura, and Insecta are epimorphic.

Ontogenetic series are available for several fossil arthropods, both stem- and crown-group. Many of these show anamorphic development and hemianamorphosis seems to be the most common mode of segmentation among stem-group taxa (e.g., Fu et al., 2014, 2018). However, segmentation in these ancient forms also exhibits some distinctive features with respect to extant taxa. Many Phosphatocopina, interpreted either as stem-group Pancrustacea (Haug and Haug, 2015) or stem-group Mandibulata (Chipman and Edgecombe, 2019), were anamorphic with indirect development (Haug and Haug, 2015), hatching as so-called head larva. In contrast to modern anamorphic taxa, no segments were added with the first few molts, that is, anamorphosis was in some way delayed. Another peculiar feature of anamorphosis in these early forms was that, similar to trilobites, segments first emerged as dorsally non-articulated units forming a single shield, the pygidium. The most anterior pygidial segments developed articulation in successive stages, in a process that in trilobites is called segment release. Trilobita, variably assigned to stem-group arthropods, stem-group chelicerates or stem-group mandibulates (Giribet and Edgecombe, 2019), mostly developed hemianamorphically (Hughes et al., 2006). However, some Emuellidae, with more than 100 trunk segments as adults, were possibly euanamorphic (Paterson and Edgecombe, 2006), whereas Zhang and Clarkson (2009) made the case for an epimorphic eodiscoid species. Delayed anamorphosis might have characterized trilobite post-embryonic development as well. Evidence for an even earlier phase of cephalic segment addition (during the so-called phaselus stage, if this was actually a phase of trilobite ontogeny), is weak (Hughes et al., 2006).

Phylogenetic distribution of anamorphosis in extant taxa and information from extinct forms concur to indicate hemianamorphic development as the primitive condition in arthropods (Hughes et al., 2006; Minelli and Fusco, 2013; Miyazawa et al., 2014; Haug and Haug, 2015; Brenneis et al., 2017). Uncertainties on key nodes of arthropod phylogeny and incomplete information on post-embryonic segmentation in several taxa prevent a formal analysis of the evolution of this developmental character at the level of the whole clade. However, starting from the hypothesis of hemianamorphosis as the plesiomorphic condition and complementing the phylogenetic distribution of the character in Figure 1 with some available information at lower taxonomic level, four different evolutionary transitions can be recognized.

Anamophosis and epimorphosis are not fundamentally distinct developmental modes, the latter being only the lower extreme degree of the former. This is more than an arithmetic truism. In several clades, e.g., in decapod crustaceans, segment number is the same in anamorphic and epimorphic lineages. Among the most polymeric epimorphic clade, the Geophilomorpha, Brena and Akam (2013) discovered a minimal leftover of anamorphosis in the species Strigamia maritima, where 2–3 terminal segments (out of 48–54 trunk segments) are added after hatching, during the first embryoid stages (see below). However, the opposite evolutionary transitions, embryonization vs. de-embryonization of segment formation, might not have the same evolvability, the former having apparently occurred more often than the latter.

In anamorphic development, as well as in embryonic sequential segmentation, the new segments appear sequentially in anteroposterior progression from a subterminal region referred to as “segment addition zone” (SAZ; Janssen et al., 2010). This is also often referred to as the proliferative (or generative, or growth) zone, but SAZ is to be preferred because it makes no assumption of localized and continuous cell proliferation in the posterior of the body (Clark et al., 2019; see also Fusco, 2005). However, information about morphogenesis and gene expression associated with anamorphosis is scarce, and current investigations are mainly concerned with the evolution of embryonic simultaneous segmentation from embryonic sequential segmentation in insects.

Evidence of a conserved role of the segment polarity gene engrailed during anamorphosis was found in the anostracan crustaceans Artemia and Thamnocephalus (Manzanares et al., 1993; Constantinou et al., 2020), in the thecostracan crustacean Sacculina (Gibert et al., 2000) and in the centipede Lithobius (Bortolin et al., 2011).

The involvement of Notch signaling is increasingly emerging as a common feature of sequential segmentation throughout the Bilateria. Williams et al. (2012) showed that blocking Notch signaling causes a specific, repeatable effect on segmentation in Artemia franciscana and Thamnocephalus platyurus, although the observation that loss-of-function Notch phenotypes differ significantly across arthropods suggests some variation in the role of Notch in the regulation of sequential segmentation.

Despite the paucity of experimental data on the developmental genetics of anamorphosis, some indirect information can be obtained from comparative studies on embryonic segmentation. In a certain way, the evolutionary embryonization of anamorphosis can be seen as a natural experiment, where post-embryonic segmentation, a process not easily accessible to current molecular methodologies, is brought under the eye of the investigator. The extended similarities found in embryonic sequential segmentation in lineages that independently evolved either complete or partial embryonization of segmentation can perhaps indicate a common basic mechanism among lineages with different degree of anamorphosis up to epimorphosis. This could be based on the same clock-and-wavefront mechanism inferred from data on embryonic segmentation in a small number of model species, and hypothesized to be ancestral and conserved among arthropods (Clark et al., 2019).

It is not always the case that hatching separates embryonic from post-embryonic phases neatly. More or less embryo-like (embryoid) hatchlings are described for many arthropod groups, under a variety of taxon-specific terms (Minelli et al., 2006; Minelli and Fusco, 2013; Fritsch and Richter, 2015; Haug, 2020; Supplementary Table 1).

Focusing on taxonomic distribution and morphological and functional characteristics of these embryoid stages, three facts highlight the evolutionary flexibility of arthropod developmental schedules. First, conditions at hatching are often different between closely related taxa (e.g., in many spiders there is a pronymph with incompletely articulated appendages, but not in all). Second, this diversity is associated with a diversity in the number of molts the animal undergoes before and after the beginning of its active life. In most pterygote insects, three embryonic cuticles are shed before hatching, but only two in the cyclorrhaphous flies (Konopová and Zrzavý, 2005). Third, the condition at hatching is not necessarily correlated to segmentation schedule. For example, epimorphic hexapod hatchlings are anything between an active juvenile and a vermiform pronymph, while anamorphic myriapods hatch in conditions so different as the very active larva I of Lithobius and the motionless pupoid of Pauropus (Minelli et al., 2006).

Situated at one extreme of both embryonic and post-embryonic phases, where the methodologies used in the study of each phase are less effective, development around hatching time is little investigated, and recent work is disclosing unsuspected situations. For example, two embryoid stages were traditionally reported for the geophilomorph centipedes, whereas a recent closer scrutiny in Strigamia maritima revealed five stages (Brena, 2014).

Many arthropods, in particular among the Pancrustacea, begin post-embryonic life as larvae. However, the term larva has been applied to immatures with very different, although non-mutually exclusive characteristics. These include forms that differ morphologically from the adult, have different ecological niches than the corresponding adult, or transform into an adult by a metamorphosis (see Haug (2020) for a detailed account), thus the qualification of development as either direct or indirect is somehow a matter of degree or requires qualitative specification (e.g., for some intermediate cases Fritsch et al. (2013) introduced the term pseudo-direct development). The evolution of post-embryonic segmentation, although potentially independent from other developmental features of juvenile stages, can be found to be variably associated to larval evolution, as for instance when the evolution of direct development coincides with a transition to epimorphosis.

Description and comparative analysis of anamorphosis assume that we are dealing with unambiguously countable units, the segments. However, not all putatively segmental structures (especially those of internal anatomy) are in register, as they can have different period or phase. Thus, a more realistic depiction of arthropod body organization is obtained by dissociating the serial homology of individual periodic structures (e.g., legs or sclerites), or segmentation, from the concept of the segment as a body module (e.g., Budd, 2001; Minelli and Fusco, 2004; Fusco, 2005, 2008; Fusco and Minelli, 2013; Hannibal and Patel, 2013). This accounts for the occurrence of so-called “segmental mismatch,” i.e., the discordance between different segmental series within the same animal, and of a number of segmental abnormalities (Leśniewska et al., 2009), but also for the high disparity in arthropod segmental patterns. The study of anamorphosis cannot disregard the complexity and the disparity of the segmentation process (Minelli, 2020).