Multiple Origins of Feeding Head Larvae by the Early Cambrian

Canadian Journal of Zoology

Multiple origins of feeding head larvae by the Early Cambrian

Journal: Canadian Journal of Zoology

Manuscript ID cjz-2019-0284.R1

Manuscript Type: Review

Date Submitted by the 15-Apr-2020 Author:

Complete List of Authors: Strathmann, Richard; Friday Harbor Laboratories and University of Washington Department of Biology,

Is your manuscript invited for consideration in a Special Zoological DraftEndeavors Inspired by A. Richard Palmer Issue?:

Cambrian, DEVELOPMENT < Discipline, EVOLUTION < Discipline, LARVAE Keyword: < Discipline, marine, planktotrophy

Multiple origins of feeding head larvae by the Early Cambrian1

Richard R. Strathmann

Friday Harbor Laboratories, 620 University Road, Friday Harbor, WA 98250 USA

[email protected]

1This review is one of a series of invited papers arising from the symposium “Zoological

Endeavours Inspired by A. Richard Palmer” that was co-sponsored by the Canadian Society of

Zoologists and the Canadian Journal of Zoology and held during the Annual Meeting of the

Canadian Society of Zoologists at the University of Windsor, Windsor, Ontario, 14–16 May 2019. Draft

Abstract: In many animals the head develops early, most of the body axis later. A larva composed mostly of the developing front end therefore can attain mobility and feeding earlier in development. Fossils, functional morphology, and inferred homologies indicate that feeding head larvae existed by the Early Cambrian in members of three major clades of animals: ecdysozoans, lophotrochozoans, and deuterostomes. Some of these early larval feeding mechanisms were also those of juveniles and adults (the lophophore of brachiopod larvae and possibly the ciliary band of the dipleurula of hemichordates and echinoderms); some were derived from structures that previously had other functions (appendages of the nauplius). Trochophores that swim with a preoral band of cilia, the prototroch, originated before divergence of annelids and molluscs, but evidence of larval growth and thus a prototrochal role in feeding is lacking for molluscs until the Ordovician. Feeding larvae that definitelyDraft originated much later, as in insects, teleost fish, and amphibians, develop all or nearly all of what will become the adult body axis before they begin feeding. On present evidence, head larvae, including feeding head larvae, evolved multiple times early in the evolution of bilaterian animals and never since.

Key words: Cambrian, development, evolution, larvae, marine, planktotroph

Introduction

Marine larvae differ in form from later juvenile and adult stages and differ among major

clades of animals. Origins of feeding larvae are of special interest because feeding requires more

elaborate structures than does motility and because larval feeding enables development from a

smaller egg or to a larger juvenile or both (Pernet 2018). Diverse kinds of feeding larvae are of

ancient origin, but inferences on their antiquity have varied widely. The times of origin,

frequency of origin, and derivation of structures for larval feeding are related issues. Most recent

studies of early larval origins have emphasized molecular genetic evidence for homology,

convergence, or divergence in development (e.g., Raff 2008; Arenas-Menas 2010; Hejnol and

Vellutini 2017; Marlow 2018; Gąsiorowski and Hejnol 2019). Fossils also provide evidence on early evolution of larvae (e.g., Nützel 2014;Draft Zhang et al. 2010, 2018). This discussion adds functional requirements for larval feeding and therefore focuses on groups with both a fossil

record and living representatives.

Some feeding larvae of bilaterian animals develop much of the larval body from what

will become the anterior part of the later juvenile and adult. Some of these larvae have been

called head larvae. Walossek and Müller (1993) used the term head larva in reference to the

crustacean head specifically, but the term has since been applied more broadly to larvae that

swim or feed with anterior structures before the trunk has formed (Lacalli 2005; Gonzalez et al.

2017) (Fig. 1). However, what is called a head and the extent of posterior development of the

larva differs among animals. Although a more general name would be front-end larva, here I

have used the term head larva in a broad sense. Though differing in extent of anterior to posterior

development, head larvae nevertheless contrast with larvae that have formed all or nearly all of

the eventual adult body axis when they initiate feeding.

Head larvae develop with little expression of Hox genes because they begin mobility and

4 feeding before posterior body parts have developed (Lacalli 2005; Hejnol and Vellutini 2017;

Gąsiorowski and Hejnol 2019, 2020). The absence of posterior parts accounts for these larvae being “the other body plan” (Raff 2008). Head larvae occur in all three major branches of bilaterian evolution, the ecdysozoans, lophotrochozoans, and deuterostomes (Walossek and

Müller 1990; Lacalli 2005).

Where head larvae and larvae composed of more of the body axis occur in the same clade, the head larvae are more broadly distributed among lineages, which suggests an earlier origin. Estimated times of origin of feeding head larvae can be especially early, but how early?

In four clades the evidence for early origins of feeding larvae includes informative fossils as well as extant larval forms. These clades are the Crustacea, Brachiopoda, Ambulacraria (Echinodermata + Hemichordata), and Mollusca.Draft Extant animals provide evidence for traits of their common ancestor (the common ancestor of the crown group), but the traits of that common ancestor originated in earlier ancestors prior to the crown group (in the stem group). Inferences for origins of larval traits therefore require evidence beyond traits of existing larvae. The evidence and therefore the basis of inferences for origins of feeding larvae differs for each clade

(Table 1). For crustaceans, evidence includes a body fossil. For brachiopods there are indications of larval growth in the larval shells remaining at the umbos of fossil brachiopod shells. For the

Ambulacraria, there are inferred homologies of extant larvae that are necessarily feeding larvae and the first appearances of fossils of adults in a clade inferred to have had such a larva. For molluscs, one of the ciliary bands used for feeding is also used for swimming; homology is uncertain for the additional bands required for feeding; larval shells are not preserved in the early fossils; and larval feeding might have originated somewhat later.

The times of origin that are indicated by this evidence are contrasted with hypotheses for later or earlier origins of feeding larvae. Also discussed are apparent similarities and differences

for origins of feeding larvae in several other taxa, including those that are not head larvae.

Crustacean nauplius

Fossil evidence of an early origin of feeding larvae is most direct for crustaceans and

their stem group. The nauplius of crustaceans is a head larva. The nauplius can begin feeding

when only the three most anterior pairs of appendages are functional: the antennules, antennae,

and mandibles (Fig. 1A) (Sanders 1963a,b). With addition of appendages posteriorly, but

continued use of naupliar structures for feeding, the larva becomes a metanauplius. With further

development, the anterior appendages change form and function, and food is no longer acquired

by the naupliar feeding mechanism (Martin et al. 2014).

Antiquity of feeding nauplii. Fossil larvae from the Early Cambrian include a metanauplius stage; structures that indicateDraft that this larva fed like a nauplius are the labrum and basal medially directed spines on the second antenna and mandible (Fig. 2) (Zhang et al. 2010).

Although the hypostomal spine and pair of eyes are not features of extant nauplii, extant nauplii

possess similar structures for feeding (Sanders 1963a; Ferrari et al. 2011). This early

eucrustacean larva is from the Yu’anshan Formation, which may correlate with late Atdabanian

(Cambrian Stage 3) (Zhang et al. 2010; Yuan et al. 2011).

Other fossil evidence for an early origin of feeding nauplii is from the feeding head

larvae of the extinct phosphatocopines, if the phosphatocopines are related to eucrustaceans as a

sister group rather than nested within them. The phosphatocopine larvae had naupliar structures

for feeding (Maas and Waloszek 2005; Zhang et al. 2012; Haug et al. 2013; Eriksson et al.

2016). The phosphatocopine larvae differ from the eucrustacean nauplius in having initially four

pairs of appendages instead of three, but the labrum and the spines at the base of second antennae

and mandibles of their head larvae are inferred to be homologous (Siveter et al. 2001; Maas and

Waloszek 2005). Fossils, inferred homologies, and inferred relationships therefore indicate that

6 the feeding mechanism of the crustacean nauplius had evolved before the common ancestor of eucrustaceans.

Derivation of structures for naupliar feeding. Initiation of motility and feeding with only the anterior appendages present may be an ancestral trait for euarthropods. Head or front-end larvae occur in such distantly related groups as trilobites, pycnogonids, and crustaceans. What is inferred to be the feeding larva of an Early Cambrian short-great-appendage arthropod had developed more than the head appendages but had not completed development of the trunk appendages (Liu et al. 2016). The initially functional anterior appendages differ greatly among euarthropods, however.

Inferred phylogenies, extant forms, and Cambrian fossils indicate the assembly of traits of the crustacean nauplius (Fig. 3). The Draftenditic spines at the base of the second antenna and mandible that contribute to the naupliar feeding mechanisms evolved in the eucrustacean stem group (Walossek and Müller 1990, 1993; Maas et al. 2003; Haug et al. 2010a,b; Zhang et al.

2012). The labrum of nauplii is a fleshy lobe with muscles and glands. The naupliar kind of labrum evolved in the common ancestor of eucrustaceans + phosphatocopines (= Labrophora); fossils of feeding larvae from the eucrustacean stem group had a minimum of four pairs of appendages, with the number subsequently reduced to the anterior three pairs in the eucrustacean crown group (Walossek and Müller 1990; Maas et al. 2003; Maas and Waloszek 2005; Zhang et al. 2012).

The earliest crustacean nauplii were not necessarily planktonic. The habitat of fossil nauplii and metanauplii appears to be uncertain. Today, some feeding nauplii are planktonic (as in barnacles and calanoid copepods) and some benthic (as in cephalocarids and many harpacticoid copepods), and the naupliar appendages gather food in diverse ways (Sanders

1963a; Dahms 2000).

Single origin of naupliar feeding. Did feeding nauplii evolve only once? Feeding nauplii

are widespread among crustaceans (Martin et al. 2014). Although nauplii are diverse (Sanders

1963a,b; Dahms et al. 2006), to my knowledge homology of the naupliar structures for feeding

has not been doubted. Not all nauplii feed, however. Have structures for feeding been lost and

naupliar feeding then regained? The first instars in development of nauplii are non-feeding in

many crustaceans. Examples include the first nauplius of thoracican barnacles and the first two

or three nauplius stages of many copepods, but the later stages feed with the usual equipment. In

contrast, nauplii in some clades, as in rhizocephalan barnacles (Høeg and Lützen1995) and

malacostracans (Scholtz 2000), do not feed at any stage. In many malacostracans, the nauplius is

embryonized as a prehatching stage. In the euphausiids and dendrobranchiate decapods, however, larvae hatch as a free naupliusDraft that swims but does not feed. Under a variety of published phylogenies, either free nauplii evolved at least once within the malacostracans or egg

nauplii evolved multiple times (Strathmann and Eernisse 1994). Scholtz (2000) considers the

evolutionary resurrection of a free nauplius from an egg nauplius to be a plausible hypothesis, in

part because so little is required of a swimming but non-feeding nauplius. The free nauplii of

euphausiids and dendrobranchiate shrimp lack a labrum, midgut, articulation of the limbs, basal

spine on the second antenna, and mandibular gnathobase, among other structures (Scholtz 2000).

Jirikowski et al. (2015) describe the shifts in timing of development that would be necessary for

restoration of a swimming nauplius from an embryonized nauplius. Loss of structures for feeding

also occurs in the evolution of non-feeding nauplii from feeding nauplii, however, and is not

necessarily an indication of an ancestral embryonized nauplius (Akther et al. 2015). In any case,

there is as yet no evidence for restoration of a feeding nauplius after loss of the structures

necessary for feeding. There is no apparent way for selection to restore structures for naupliar

feeding once they are lost from all developmental stages. Existing evidence points to a single

8 origin of feeding nauplii and several irreversible losses of a feeding nauplius (Martin et al. 2014).

Brachiopod larvae.

Of the three extant groups of brachiopods (Linguliformea, Craniiformea, and

Rynchonelliformea), it is the linguliform brachiopods that have feeding larvae (Fig. 4). Of the linguliform brachiopods, the discinids initiate development of their shells after feeding begins

(Fig. 5), and the lingulids initiate development of shells before the larvae begin to feed (Chuang

1977; Nielsen 1991; Freeman and Lundelius 1999). The non-feeding larvae of extant craniiform and rhynchonelliform brachiopods do not form shells until settlement and metamorphosis.

Antiquity of feeding brachiopod larvae. In linguliform brachiopods, both discinids and lingulids, the larval shells increase in size as the larvae grow. The shells of the feeding larvae are retained through metamorphosis so that Draftthey persist in intact shells of postlarval juveniles. A change in form or structure of a fossil shell can indicate the end of the larval stage and beginning of life as a benthic juvenile (Holmer 1989; Freeman and Lundelius 2005; Zhang et al. 2018).

Evidence for larval growth and therefore larval feeding is deposition of shell between the initial shell and a discontinuity indicating metamorphosis (Fig. 6). The size of the shell formed before inferred metamorphosis is another indication of growth and therefore feeding.

A feeding larva has been inferred from fossil brachiopods of the Early Cambrian. The variety of early lineages with feeding larvae indicates that the ancestor of brachiopods had feeding larvae (Freeman and Lundelius 1999; Balthasar 2009; Holmer et al. 2009; Skovsted et al.

2015; Ushatinskaya 2016; Zhang et al. 2018). One of the earliest brachiopod fossils with indications of a feeding larva is a Pelmanotreta species from the Tommotian (Cambrian Stage 2)

(Skovsted et al. 2014).

The tommotiids are known as shelly fossils from the Cambrian. Under an interpretation of the tommotiids as stem brachiopods, a larva with a bivalved shell preceded the evolution of an

adult with a bivalved shell (Larsson et al. 2014). Murdock et al. (2014) criticized the hypothesis

as being based on brachiopods as an interpretative model but did not reject it. The hypothesis

that tommotids included stem brachiopods with a bivalved feeding larva may be tested through

further research (Harper et al. 2017).

Derivation of structures for brachiopod larval feeding. The structures that larvae of

ancestral brachiopods used for feeding are not preserved. Presumably they fed and swam with

lophophores as extant feeding larvae do. Larvae of linguliform brachiopods possess the same

frontal, laterofrontal, and lateral ciliary bands on their tentacles as adult brachiopods (Strathmann

2005) (Fig. 4, 7), and the tentacles of linguliform larvae are retained through metamorphosis.

Both larvae and adults capture phytoplankton and other small suspended particles. The simplest hypothesis is that the ciliary bands and feedingDraft mechanism were an ancestral trait. The same ciliary bands occur in larval and adult phoronids (Riisgård 2002). The phoronids are inferred to

be the sister group of brachiopods (Sperling et al. 2011; Kocot et al. 2017) (Fig. 4). Feeding

larvae of extant linguliform brachiopods swim, are collected in plankton nets, and are therefore

inferred to be planktonic rather than benthic. Differences between larval and adult shells of fossil

brachiopods suggest similarity in the use of different habitats by these stages from the origin of

brachiopods.

Extension and orientation of the lophophore for swimming and a low density relative to

seawater are the primary requirements for a planktonic rather than a benthic life for the larvae.

Long larval setae are a defense for early stage larvae of extant discinid brachiopods (Chuang

1977) and may have been a defense for planktonic larvae of the earliest known brachiopods.

The larvae of linguliform brachiopods initiate feeding with tentacles of the lophophore,

which are anterior and develop early, whereas the pedicle, which is posterior, appears later in

larval development (Chuang 1977; Long and Stricker 1991; Freeman 2007; Zhang et al. 2018).

Larvae of Disciscina initially have a lophophore and setae but no shell (Fig. 5). Expression of head and neuronal marker genes in lophophores of a brachiopod (Lingula) and in the closely related Phoronida (Phoronis) resembles gene expression in heads of other bilaterians (Luo et al.

2018), and in phoronids larvae develop to stages with lophophores without Hox gene expression

(Gąsiorowski and Hejnol 2020). Larval brachiopods initiate feeding as head larvae or at least as front-end larvae but with surface structures differentiated as far posterior as the setae.

Number of origins of feeding brachiopod larvae. The similarity of larval and juvenile brachiopods suggests that planktonic feeding larvae could be derived from benthic juveniles

(Strathmann 1993), and evidence for separate origins of larval feeding before metamorphosis could be sought among fossil brachiopods. To my knowledge, however, there is as yet no evidence that feeding brachiopod larvaeDraft evolved more than once. For conversion of the lophophore of a benthic juvenile into a lophophore for a planktonic feeding larva, the lophophore would need to be modified for swimming. Swimming depends on a lophophore that can extend beyond the shell and change position of tentacles to change direction of swimming (Fig. 5). Once premetamorphic development of a lophophore has been lost, selection might not favor development of a lophophore in the larval stage because the postlarval lophophore is unsuitable for swimming.

Brachiopod larvae in the Early Cambrian are inferred to have had shells and arrangements of setae and other structures different from those of extant feeding larvae

(Balthasar 2009; Skovsted et al. 2014; Ushatinskaya 2016; Zhang et al. 2018). Shells of extant brachiopod larvae resemble post-larval shells. Also, setae of some non-feeding larvae of rhynchonelliform and craniiform brachiopods are secreted solely by the chaetoblast whereas setae of larvae and adults of a lingulid brachiopod are secreted by both chaetoblast and follicle cells (Lüter 2000). Setae of a discinid were formed largely by the chaetoblast at the earliest larval

stage but with a greater contribution of follicle cells later (Lüter 2001). Discinid larvae at later

stages and lingulid larvae have been described as swimming juveniles (Long and Stricker 1991;

Lüter 2000, 2001; Zhang et al. 2018), but this designation ignores use of the lophophore for

larval swimming (Santagata 2011) and the initial lack of a shell and the earliest developing setae

in the discinid larvae. Differences in shells between feeding larvae of the Early Cambrian and

those today could represent shifts in timing of development of structures to an earlier stage

(Zhang et al. 2018). Similar shifts are known for other larval forms, for example the early

development of a skeleton in pluteus larvae of echinoderms (Shashikant et al. 2018).

Loss of larval feeding in rhynchonelliform brachiopods. One hypothesis for the absence

of feeding larvae in extant rhynchonelliform brachiopods is the selective extinction of species with feeding larvae at the end of the PermianDraft and in the Early Triassic (Strathmann 1978b; Valentine 1986). The Permian-Triassic mass extinction provides a model for possible future

events. This mass extinction was associated with increased carbon dioxide from extensive

volcanism, with resulting global warming, ocean acidification, hypoxia, anoxia, and toxic sulfide

(Knoll et al. 2007; Payne and Clapham 2012). These are among the conditions that we are

producing now, though we are contributing additional changes, such as novel organic materials.

Valentine (1986) calculated that given the magnitude of extinctions within clades, a moderately

selective extinction could eliminate all species with feeding larvae.

The rhynchonelliform brachiopods that survived the Permian-Triassic extinctions to leave

descendents today were all in a clade with a common ancestor in the early part of the Paleozoic

(Carlson 2016). Because of a reversal of mantle lobes at metamorphosis that is peculiar to their

clade (Long and Stricker 1991), those rhynchonelliforms are inferred to have inherited a non-

feeding larva from that ancient ancestor (Freeman and Lundelius 2005). Because of traces of

larval shells in fossils, other clades of rhynchonelliform brachiopods in the Paleozoic are inferred

12 to have had feeding larvae (Freeman and Lundelius 2005). These observations, by themselves, are consistent with selective extinction of species with feeding larvae. However, linguliform brachiopods survived the end-Permian and Early Triassic extinctions. Shells of Paleozoic linguliforms indicate feeding larvae (Freeman and Lundelius 1999), and extant linguliform brachiopods have feeding larvae (Fig. 5, 7). Linguliform brachiopods were a relatively abundant part of the fauna during the harsh conditions in the Early Triassic (Peng et al. 2007; Posenato et al. 2014; Chen et al. 2015). Differences in extinction and survival of rhynchonellforms and linguliforms have been attributed to features unrelated to larval feeding, such as different materials in shells (Peng et al. 2007; Posenato et al. 2014).

Ambulacrarian dipleurula The hemichordates and echinodermsDraft form a monophyletic group, the Ambulacraria (Cannon et al. 2014; Simakov et al. 2013; Cannon et al. 2014; Peterson and Eernisse 2016) (Fig.

4). The feeding larval forms of enteropneust hemichordates and of four classes of echinoderms have different names: the tornaria (enteropneust hemichordates), bipinnaria (asteroids), ophiopluteus (ophiuroids), echinopluteus (echinoids), and auricularia (holothuroids). For convenience, these feeding larval forms can be lumped under the name dipleurula. Crinoids are sister to the other extant echinoderm classes and, so far as is known, lack feeding larvae today, although retention of an auricularia-like stage of a stalked crinoid indicates a feeding dipleurula in their past (Nakano et al. 2003). The name dipleurula was previously used as the name of a hypothetical ancestral form. The name has also been used for only the tornaria, auricularia, and bipinnaria because, at early stages, these larvae are especially similar in form (Fig. 8ABC).

However, all of the feeding larvae of echinoderms and hemichordates are sufficiently similar in form and feeding mechanism that a group name is needed, and dipleurula is used here. All of these larvae are suspension feeders. They capture phytoplankton and other small particles with a

band of simple cilia that beat away from a circumoral field (Fig. 7, 8ABC). Food particles are

captured on the upstream side of that band and conveyed to the mouth, in part by brief local

reversals of beat of the ciliary band that are induced by encounter of cilia with the particle (Fig.

8C) and to varying extents by the action of cilia of the circumoral field and around the mouth

(Strathmann 1971; Strathmann and Bonar 1976; Hart 1991; Hart et al. 1994; Hart 1996a;

Strathmann 2007). Another feature shared by the dipleurulae of the Ambulacraria is a gel filled

primary body cavity that maintains a complex larval shape despite a body wall that is mostly a

very thin epithelium (Strathmann 1989).

Antiquity of the dipleurula. Inferences on time of origin of dipleurulae depend on inferred

homologies of structures involved in larval feeding. The function of the ciliary band in feeding and swimming indicates that an ancestralDraft dipleurula could originate only in association with feeding. A ciliary band that surrounds a circumoral field is required for feeding, but along much

of a band in this position the cilia are not producing a current from front to back. Use of the

ciliary band for swimming is compromised. In the auricularia and bipinnaria, the band is angled

on lobes so that there is an anterior to posterior component to the current along much of the

band, despite the cilia beating perpendicular to the band and away from the circumoral field, but

the ciliary current is not directly from anterior to posterior along much of the band (Strathmann

1971). In the ophiuroids (Fig. 7) and echinoids stability in shear is aided by angles of the arms

that direct the current laterally as well as posteriorly (Grünbaum and Strathmann 2003;

Strathmann and Grünbaum 2006). In swimming but non-feeding ambulacrarian larvae, cilia

produce currents more directly from anterior to posterior rather than laterally (Emlet 1991,

1994). The continuous ciliary band of the auricularia, a feeding stage, transforms into a series of

transverse rings in the subsequent non-feeding doliolaria stage (Fig. 8D). The rearrangement into

transverse bands confers greater swimming speed before settlement. In the tornaria, a posterior

14 ring of cilia that does not catch particles produces a current for swimming; the looping ciliary band captures food but contributes little to swimming (Strathmann and Bonar 1976).

If feeding larvae of the Ambulacraria are derived from a common ancestor with a similar feeding larva, then the latest time of origin of larval feeding in this clade is shown by divergences between clades that now have feeding larvae (Strathmann 1993). Fossils of adults indicate a divergence by the Early Cambrian. Fossil echinoderms are known from the

Atdabanian (Cambrian Stage 3) (Zamora et al. 2013; Kouchinsky et al. 2015), and a fossil from

Cambrian Stage 1 has been interpreted as an echinoderm (Topper 2019). A fossil interpreted to be a pterobranch hemichordate is from the Atdabanian or possibly early Botomian (Cambrian

Stage 3) (Hou et al. 2011), although its identity as a hemichordate has been doubted (Maletz 2019). A still earlier estimate for this divergenceDraft is from molecular clocks, which have indicated divergence of hemichordates and echinoderms in the Ediacaran (Erwin et al. 2011), and hence a much earlier origin of the dipleurula as a feeding larva.

Derivation of ciliary feeding by dipleurulae. The tornaria larva of enteropneusts is a head larva (Lacalli 2005; Gonzalez et al. 2017). At metamorphosis, the front part of the juvenile and adult body, as far posterior as the pharyngeal openings, develops from the larval body (anterior to its telotroch); development of the more posterior part of the juvenile and adult body is by posterior extension (Lacalli 2005; Urata and Yamaguchi 2004; Gonzalez et al. 2017) (Fig. 1).

Gonzalez et al. (2017) concluded that the early tornaria larva is transcriptionally similar to a truncated version of the adult, where most of the ectoderm has the same molecular signature as the proboscis and collar of the adult, and lacks a trunk. A narrow territory around the blastopore corresponds transcriptionally to the posterior tip of the adult trunk. Evolution of a feeding dipleurula thus appears to have proceeded from anterior structures that appeared early in the development of a juvenile stage. The inferred homologies between feeding larvae of

enteropneust hemichordates and echinoderms implies that echinoderm larvae were derived from

an ancestral head larva, although that derivation has been obscured by varying changes in

development that accompanied changes in postlarval structures of echinoderms (Cameron et al.

2006; Hara et al. 2006; Mooi and David 2008; Smith 2008; Lacalli 2014; Kikuchi et al. 2015;

Byrne et al. 2016; Szabó and Ferrier 2018). If a larval form originates from the first

differentiating anterior structures of an ancestor with a head, it is still a head larva later when the

adult no longer has a recognizable head.

The precursor of the ciliary band of the dipleurula is uncertain, as is also the form of the

common ancestor of the Ambulacraria. The structures for feeding by dipleurulae may have

originated from structures that previously developed in benthic juveniles; but what structures were in the ancestral juvenile? The ciliaryDraft band is preoral whereas the pharyngeal openings of ambulacrarians are postoral. Presumably, the preoral ciliary band of the larva was derived from

ancestral preoral cilia that were used in feeding.

The feeding mechanism of the pterobranch hemichordates suggests one hypothesis.

Pterobranchs lack feeding larvae, as far as is known, but the adults capture particles upstream

from a band of simple cilia (Stebbing and Dilly 1972; Gilmour 1979; Lester 1985; Halanych

1993) as do dipleurulae. There are differences, however. Measurements and figures indicate

shorter lateral cilia on the tentacles of pterobranchs than in the ciliary band of the dipleurula:

about 10 to 15 µm in pterobranchs (Dilly 1972; Gilmour 1979; Halanych 1993) in contrast to

about 20 to 25 µm in larvae of echinoderms and enteropneust hemichordates (Strathmann 1971;

Strathmann and Bonar 1976; McEdward 1984; Hart et al. 1994). Also, a row of laterofrontal cilia

has been described from pterobranchs (Gilmour 1979; Halanych 1993) but is absent in

dipleurulae. It is not yet possible to compare the processes of capture and concentration of

particles by pterobranchs and dipleurulae because of insufficient observations of pterobranchs.

Stebbing and Dilly (1972), Gilmour (1979), and Lester (1985) observed ciliary currents and capture of particles upstream from the lateral band of cilia of pterobranchs, but they lacked methods for observation of ciliary behaviors. Gilmour (1979) suggested a physical mechanism that cannot account for a sufficient volume of water cleared of particles per time. Dilly (1985) observed feeding with particles (carmine and carbon) that are likely to induce rejection rather than high rates of capture. A study of ciliary feeding by pterobranchs that follows the criteria suggested by Hart (1996b) is needed for a comparison of feeding by pterobranchs and dipleurulae.

Another possibility is that the ciliary band of the dipleurula is derived from a ciliary mechanism of sorting particles near the mouth. Under this hypothesis, the ciliary band of the dipleurula evolved by extension of an ancestralDraft oral ciliation into a longer ciliary band that enabled the animal to capture scarce suspended particles of food at a higher rate. Studies of extant enteropneusts do not provide evidence of the appropriate oral cilia, however. Their preoral ciliary organ is a ciliary band near the mouth with cilia of 25µm length, but the direction of the ciliary current is toward the mouth, opposite to that in the larva (Cameron 2002; Gonzalez and

Cameron 2009).

Extant dipleurulae swim and are found in the plankton. Dipleurulae appear to have been suspension feeding swimmers from their origin to the present.

Single origin of dipleurulae. The distribution of feeding and non-feeding larval forms, inferred relationships, and the inferred single origin of a feeding dipleurula imply numerous losses of the feeding larval form (Strathmann 1974, 1978a,b; Emlet 1990; Wray 1995, 1996;

McEdward and Miner 2001; Keever and Hart 2008). A single early origin implies the subsequent loss of larval feeding in pterobranch and harrimaniid hemichordates, in crinoids, in several orders of echinoderms, and in numerous lower taxa. The inference of a single origin does not

minimize the number of evolutionary transitions between two traits (larval feeding, no larval

feeding) but the evolutionary route between feeding and nonfeeding is strongly biased. There is

no apparent route for an evolutionary transition from a non-feeding to a feeding larva once the

structures for feeding have been entirely lost. In the Ambulacraria, nearly all non-feeding larvae

lack a mouth opening, lack a ciliary band surrounding an oral field, and are greatly altered in

form (Strathmann 1978a,b; Wray 1995; McEdward and Miner 2001). Once loss of structures of

the dipleurula have progressed to this extent, there appears to be no way of going back.

Also, hypotheses of multiple origins of this kind of feeding larva do not account for

greater similarity among feeding larvae within the Ambulacraria than with any feeding larvae

outside this monophyletic group, and hypotheses of multiple origins of dipleurulae within echinoderm classes do not account for greaterDraft similarity of feeding larvae within each of the four classes of echinoderms than among classes. To support the alternative hypothesis of independent

origins and non-homology, one must account for repeated evolution of such similar kinds of

feeding larvae within a clade and never in another clade.

The feeding larvae of ambulacrarians differ between phyla in presence/absence of some

ciliary bands (telotroch, adoral band) (Strathmann and Bonar 1976). Larval nervous systems

have diverged, but more strikingly among echinoderm larvae than between the tornaria of

hemichordates and the auricularia of echinoderms (Bishop and Burke 2007; Byrne et al. 2007)

and with transitions toward a more derived condition evident within the echinoids (Bishop et al.

2013). Differences among feeding dipleurulae are unsurprising as evolutionary divergences

whereas no hypothesis has been suggested for independent origins of such features as the overall

form at early larval stages of enteropneusts, holothuroids, and asteroids.

The conclusion that there was a single Early Cambrian or Precambrian origin of the

feeding dipleurula larva depends on inferred homologies between feeding larvae of

18 hemichordates and echinoderms and on observations that their ciliated bands are suited for feeding but compromised for swimming. The different hypothesis that the dipleurula evolved early as a non-feeding larva and with later separate evolution of larval feeding in hemichordates and echinoderms, is implied by Peterson (2005) but cannot account for origin of the dipleurula’s ciliary band and form in a non-feeding larva.

Loss of larval feeding in crinoids. The Permian-Triassic extinction was a severe bottleneck for crinoids (Twitchett and Oji 2005). Extant crinoids are inferred to be a single clade descended from the survivors (Gorzelak 2018), and feeding larvae are unknown for extant crinoids. Loss of all crinoid species with feeding larvae during the Permian-Triassic mass extinction seemed a plausible explanation for absence of feeding larvae in extant crinoids (Strathmann 1978b; Valentine 1986). Nevertheless,Draft the discovery of an auricularia-like larval stage of a stalked crinoid (Nakano et al. 2003) suggests that crinoids with feeding larvae may have survived the Permian-Triassic extinctions. Although the larva does not feed, it has the form of an auricularia, which is a feeding dipleurula of holothuroid echinoderms. Other ambulacrarians that have evolved non-feeding larvae have, over time, lost the feeding larval form. As discussed above, the ciliary band of the dipleurula is an adaptation for feeding and less effective for swimming than transverse ciliary bands or broad fields of cilia on a more nearly spheroidal larva (Emlet 1991, 1994; Wray 1996). The auricularia stage of this stalked crinoid is followed by a doliolaria-like stage (Amemiya et al. 2015), with rings of cilia better oriented for swimming. In previously studied crinoids, embryos develop directly into a doliolaria. It is unexpected that the form of a non-feeding dipleurula larva would be retained for such an extended period of evolution. The non-feeding auricularia of a holothuroid has retained the larval form, but its occurrence within a genus with feeding larvae in other species indicates a shorter time since loss of the capability to feed (Emlet 2016). Alternative hypotheses for the retention of

the form of an auricularia larva in a crinoid are that (1) the loss of dipleurula traits is

extraordinarily slow in this lineage of crinoids, with the form retained for about 250x106 years,

or (2) a post-Permian ancestor of Recent crinoids had feeding larvae. The second hypothesis

implies that crinoids with feeding larvae persisted through the Permian-Triassic extinctions.

Feeding larvae appear to have been lost in the most extensively studied extant group of crinoids,

the comatulids, but there have been few studies of larvae in other extant crinoids.

Molluscan veliger

The ancestor of crown group molluscs presumably had a trochophore-like larva that

swam with a preoral band of cilia (the prototroch) because trochophores and similar larvae are

known from related phyla, such as the Entoprocta and Annelida, and trochophore-like larvae are known from most molluscan classes: theDraft Polyplacophora, Aplacophora, Scaphopoda, Bivalvia, and Gastropoda (Fig. 4). However, in most molluscan classes the larvae that swim with a

prototroch are non-feeding. Feeding veliger larvae occur only in the Gastropoda and Bivalvia,

and some of the early diverging clades within the gastropods and bivalves lack feeding veligers.

These include early diverging branches such as the Patellogastropoda, Vetigastropoda, and

Protobranchia (Fig. 4).

Extant feeding veligers capture algal cells and other small food particles between parallel

bands of cilia whose effective strokes are toward each other (Romero et al. 2010; Strathmann et

al. 2019) (Fig. 7). One band, the prototroch, is preoral, is composed of longer cilia, and produces

a current from anterior to posterior for both swimming and feeding. The other band, the

metatroch, is postoral and composed of shorter cilia. Between these bands is a ciliated food

groove. Food particles are retained between prototroch and metatroch and transported to the

mouth by cilia of the food groove.

Antiquity of feeding by veligers. The shell deposited by a veliger is often preserved at the

20 apex of the shell of a postmetamorphic juvenile (Shuto 1974; Jablonski and Lutz 1983).

Preservation of the shell deposited during larval growth indicates larval feeding. Also a small initial shell deposited during embryonic development indicates a small egg, and a sufficiently small egg indicates larval feeding. Conversely, the shell apex can indicate a lack of larval growth or a large egg, and thus indicate a lack of larval feeding. Feeding in the past was presumably by opposed prototroch and metatroch, as it is now.

Unfortunately, larval shells are not well preserved in Cambrian fossils. Nützel et al.

(2006) found that the internal casts from shells of univalved Cambrian molluscs were large

(about 100 to 300 µm at 100 µm from the apical end) but casts from Ordovician and Silurian shells were often smaller (about 20 to 120 µm at 100 µm from the apical end). They inferred a late Cambrian to Ordovician origin for larvalDraft feeding in univalved molluscs. External shell surfaces would provide stronger evidence for presence or absence of larval growth because shell can be deposited on internal surfaces later in development, changing the internal dimensions

(Freeman and Lundelius 2007), but clear evidence from external surfaces of shell apices are lacking from Cambrian molluscs (Nützel 2014). Also, if Cambrian molluscs initiated larval feeding before initiation of a shell, there would possibly not be a small shell apex. On present evidence, however, there is no certain indication of larval growth preserved in fossil molluscs from the Cambrian (Runnegar 2007).

If homology of metatroch, and food groove could be demonstrated conclusively, it would indicate an origin of opposed-band feeding before the divergence of gastropods and bivalves or even earlier before the divergence of molluscs and annelids (Nielsen 2018), but homology and homoplasy of metatrochs are both open to doubt (see below).

Derivation of feeding by veligers. As a transverse ciliary band encircling the larva, the prototroch functions well for swimming as well as for feeding. Whether a prototroch is part of an

opposed-band feeding mechanism or not, the prototroch propels the larva (Emlet 1991;

Strathmann and Grünbaum 2006). Embryos with little protection become mobile early (Staver

and Strathmann 2002; McDonald and Grünbaum 2010). The prototroch provides motility as

early as the gastrula stage. The prototroch might have evolved as a means of swimming early in

development and later became part of the opposed-band feeding mechanism. The compromises

between feeding and swimming are slight compared to those for larvae of the ambulacraria.

An annelid trochophore, whether feeding or not, is a head larva (Lacalli 2005). In

contrast, by the time veligers feed, they are clearly more than a head larva (Page 2009). Feeding

veligers have a mantle, a shell and the beginning of a foot. Nevertheless, the molluscan

prototroch was present in an ancestral trochophore stage, whether it fed or not, and the ciliation for opposed-band feeding of mollusc larvaeDraft is part of the head. Two speculative scenarios suggest ways that opposed-band feeding might evolve, starting

with an ancestor that had a non-feeding larva that was propelled by a prototroch but lacked food-

groove and metatroch. In one scenario opposed band feeding could originate in shelled but non-

feeding larvae of molluscs. Non-feeding veligers of extant patellogastropods and vetigastropods

have post-prototrochal cilia that convey particles out of the mantle cavity (Hadfield et al. 1997).

The suggestion is that post-prototrochal cilia might have been modified to become the metatroch

and food groove cilia. In this scenario, food groove and metatroch of molluscan veligers

originated after evolution of the larval shell and therefore after the larva was no longer a head

larva. A second scenario is based on feeding trochophore larvae of annelids and could account

for an earlier origin of opposed-band feeding in a shell-less head larva. The scenario is suggested

by the diverse methods of feeding by annelid trochophores. Some feeding trochophores of

annelids capture relatively large food items one at a time (Phillips and Pernet 1996). Other

annelid trochophores capture relatively large food items but also capture small algal cells with

22 opposed prototroch and metatroch (Miner et al. 1999). Still other annelid trochophores with opposed prototroch and metatroch capture only smaller food (Pernet 2018). The suggested scenario is that opposed-band feeding by trochophores evolved first by elaboration of oral cilia to capture particles and then by extension of this ciliation to form the metatroch and food groove

(Miner et al. 1999). There is little supporting evidence for either of these evolutionary scenarios, but they suggest transitions that could bridge the gap between a non-feeding larva swimming with a prototroch and a larva feeding with opposed bands.

Number of origins of feeding veligers. Authors differ widely in inferences of single or multiple origin of the metatroch and food groove. An origin of feeding by veligers near the

Cambrian-Ordovician boundary (Nützel et al. 2006; Nützel 2014) implies at least two origins of the opposed-band feeding mechanism inDraft molluscs because ancestors of gastropods and bivalves had diverged by then. At another extreme, some authors inferred homology and a single origin for the metatrotroch and food groove because of the striking similarities in structure and function of metatroch and food groove as parts of an opposed-band feeding mechanism in molluscs, annelids, and some other lophotrochozoan phyla (Hatschek 1878. 1880; Jägersten 1972, Nielsen

1987, 1998, 2009, 2012, 2018). An alternative hypothesis, however, is that presence of a prototroch is a precondition that increases chances for subsequent evolution of metatroch and food groove (see above). Molluscan veligers differ from ambulacrarian dipleurulae in that the prototroch is, by itself, well suited for swimming as well as being part of the opposed-band feeding mechanism, whereas the ciliary band employed by feeding dipleurulae is not well suited for swimming. Feeding and non-feeding larvae of molluscs often remain similar whereas non- feeding larvae of ambulacrarians diverge from the forms of feeding larvae. Convergence on the opposed-band feeding mechanism is unproven but is at present a plausible hypothesis.

Demonstration of homology of metatrochs and food grooves would demonstrate a very

early origin of the feeding mechanism (Nielsen 1998, 2018) (Fig. 4), but evidence is not

decisive, both for and against. Cell lineages for metatrochs are sufficiently diverse even within

caenogastropods that cell lineages are unhelpful (Gharbiah et al. 2013). Differences between

annelids and molluscs in metatrochal arrests during prototrochal beat are consistent with separate

origins of their metatrochs but separate origins are not the only possible cause (Strathmann et al.

2019).

Some inferences of multiple origins of opposed-band feeding have been based on

minimizing the numbers of evolutionary transitions (losses and gains of metatroch and food

groove) (Haszprunar et al. 1997; Rouse 1999, 2000), the evidence being a phylogeny and the

distribution of the traits in extant species. A single origin of opposed-band feeding implies numerous later losses of metatroch and Draftfood groove, overall or within molluscs and within annelids. To be convincing, however, such inferences need an estimate of probabilities of

evolutionary transitions (Keever and Hart 2008), and there is as yet no way to estimate relative

probability for loss and gain of a metatroch.

If other evidence is found for single or multiple origins of metatrochs, stronger inferences

on the antiquity and therefore derivation of opposed-band feeding may be possible. On present

evidence, one cannot reject the hypotheses that opposed-band feeding evolved separately in

annelid head larvae and in molluscan whole-body larvae and multiple times in molluscs.

Similarities and contrasts for other larval origins

Origins of other kinds of feeding larvae provide context for the early origins of feeding

head larvae that have been discussed thus far.

Whole-body larvae. There is support for the hypotheses that (1) feeding head larvae

evolved early in the diversification of bilaterians and (2) feeding larvae that evolved later initiate

feeding when more of the body axis has developed. This distinction corresponds to some

24 definitions of primary and secondary larvae (Marlow 2018). Feeding larvae that are clearly not head larvae include those of holometabolous insects (Nel et al. 2013; Truman and Riddiford

2019) and amphibians (Schoch 2009), with origins by the Carboniferous. Teleost fish originated perhaps as early as the Carboniferous or Permian (Hurley et al. 2000), and the Elapomorpha, with the distinctive leptocephalus larva, is the inferred sister group to other crown group teleosts

(Friedman 2015). A fossil series of developmental stages of an upper Devonian stem lamprey lacked an ammocoete larva, indicating a later origin for this larval form (Miyashita 2018).

There may be cases, however, in which the supposed primary feeding larvae originated later than the Cambrian or secondary feeding larvae originated in the Cambrian. Difficulties in estimating times of larval origin are absence of fossils of the larvae, uncertainty about time of origin of the common ancestor of extantDraft animals that have the larva, and uncertainty about presence or absence of the larva in the lineage prior to that common ancestor. In other words there is often uncertainty about time of origin of the crown group and presence or absence of the larva in the stem group. Some examples follow.

Some distinctive feeding mechanisms of head larvae are restricted to a later branch within a phylum, which suggests the possibility of late times of origin. One example is the feeding mechanism of the pilidium larva, which occurs in a later branch of nemerteans. The pilidium has a uniquely different larval feeding mechanism; its feeding employs anterior structures; and its feeding is initiated before development of most of the body axis of juvenile and adult (Von Dassow et al. 2013; Maslakova and Hiebert 2014; Hiebert and Maslakova 2015).

Other examples occur among those annelids in which larvae initiate feeding before the entire body axis is formed at the trochophore or early metatrochophore stages. These larvae feed by diverse means, as in the families Polynoidae, Phyllodocidae, Nephtyidae, and Pectinariidae

(Pernet 2018). Groups with these feeding mechanisms are restricted to later branches within the

annelids (Parry et al. 2016; Weigert and Bleidorn 2016). A common feature of these annelid

larvae and the pilidium is a preoral ciliary band, an arrangement of cilia suitable for both

locomotion and feeding (Strathmann and Grünbaum 2006). It is possible that a preoral ciliary

band permits later originations of feeding mechanisms based entirely on anterior structures, with

derivation either from a swimming but non-feeding larva or from an earlier larval feeding

mechanism that employed a preoral ciliary band. I do not know of estimates of times of origin of

these larval feeding mechanisms.

On present evidence, it is possible that some larvae in which structures along much of the

body axis develop prior to feeding originated as early as the Cambrian, although that early an

origin has not been demonstrated. Possible examples occur within the annelids. Chaetopterid larvae and the pelagosphaera larva of sipunculansDraft develop much of the posterior body before initiation of feeding (Irvine and Martindale 2001; Boyle and Rice 2014). Phylogenetic inferences

from molecular data (Weigert and Bleidorn 2016) place these groups among the basal branches

for the phylum, although inferences based on morphological data place the branch to

chaetopterids in a less basal position (Parry et al. 2016). A putative fossil sipunculan is Early

Cambrian (Huang et al. 2004). These larvae, which have all or most of the body axis of the adult,

may be in groups that diverged early from other annelids, but it is not known if these kinds of

feeding larvae originated early or late in the stem preceding the crown group.

The zoea larva of decapod crustaceans has most of the adult segments when it begins

feeding. In dendrobranchiate decapods larval feeding begins at an earlier stage than in the

remaining decapods, but even in dendrobranchiates, larval feeding is initiated when much of the

body axis has developed, and the equipment for feeding differs from that of the nauplius. Fossil

larvae of decapod crustaceans are known from the Mesozoic (Haug et al. 2014). A phylogenomic

study with an estimated divergence within crown decapods as early as late Ordovician (Wolfe et

26 al. 2019) suggests a much earlier origin for a zoea-like larva.

Origin of feeding larvae of non-bilaterians (no heads). Anterior to posterior development has no role in the evolution of feeding larvae of non-bilaterians. In feeding larvae of anthozoans, the mouth is at the rear end of the swimming planula (Gemmill 1920; Pernet 2018), and at settlement the front end of the swimmer becomes the basal part of the polyp. Structures at the leading end of an animal do not feature as the structures for larval feeding as they do for head larvae.

The cydippid larva of ctenophores appears to provide an extreme example of origin of a feeding larval stage by evolutionary modification of the adult rather than the larva, a nearly

Haeckelian larval origin. The feeding cydippid larva occurs in life histories of most ctenophores and appears to be little modified from theDraft juvenile of a directly developing ancestor, but in several clades of ctenophores, the postlarval stages have evolved into different forms (Whelan et al. 2017). With little modification at early stages, the ancestral juvenile has become a larva because of evolutionary changes of the adults.

A tail larva rather than a head larva. Although non-feeding, the ascidian tadpole should be mentioned as a tail-dependent larva that metamorphoses into an adult composed mostly of anterior structures (Cloney 1982; Stolfi and Brown 2015), the reverse of evolution of larvae through early functioning of an earlier developing front end. The tadpole begins motility by swimming with a muscular tail with a dorsal nerve cord and a notochord. The tail is resorbed at metamorphosis. Feeding with pharyngeal openings is not initiated until after metamorphosis. In several species in the ascidian family Molgulidae the tail does not develop. Independently in several lineages molgulids have lost traits of their phylum without changing traits characterizing their family, and the change in body plan is not ancient (Huber et al. 2000; Wray and Strathmann

2002; Maliska et al. 2013). Although interpretation of putative tunicate fossils from the Early

Cambrian is difficult (Shu et al. 2010), present evidence does not eliminate the possibility that

the tadpole originated as early as the Cambrian.

Similarities and contrasts in origins of feeding head larvae

Times and environments of earliest origins. Although the bases of inferences and strength

of evidence differs for Crustacea, Brachiopoda, and Ambulacraria, the evidence indicates

existence of their feeding head larvae by the Early Cambrian (Table 1). That is sufficient to

reject the hypothesis that planktotrophic larvae did not evolve until the latest Cambrian or Early

Ordovician as inferred by Peterson (2005). Peterson proposed that larval planktotrophy evolved

from ancestral larval lecithotrophy as a strategy against a unique set of evolutionary and

ecological circumstances that arose in the Early Ordovician. Servais et al. (2008, 2010) concurred that larval planktotrophy originatedDraft in invertebrate larvae during the Late Cambrian- Early Ordovician as part of the Ordovician biodiversification. Feeding larvae originated in some

clades much earlier, however, and the ciliary feeding larvae were certainly planktotrophic. Some

planktotrophic larvae originated near the time that the stem groups for extant phyla and classes

were diverging.

These feeding larvae may also have originated at quite different times and thus in

different environments. Fossils provide minimal estimates of antiquity. Greater antiquity is

indicated by times of divergences of clades that are based on molecular clocks. Molecular clocks

indicate divergence of echinoderms and hemichordates in the Ediacaran (Erwin et al. 2011),

which implies an Ediacaran origin of feeding dipleurula larvae. That would put the origin of

feeding dipleurulae much earlier than the origin of feeding veligers if feeding by veligers did not

evolve until late in the Cambrian or early in the Ordovician. Alternatively, if the common

ancestor of molluscs and annelids had larvae that fed with the opposed band mechanism (Nielsen

2018), then the origin of their larval feeding could also antedate the Cambrian. An origin of

28 naupliar feeding appears to have awaited the Early Cambrian. However, arthropod larvae that had only anterior appendages for feeding and motility preceded evolution of the kind of labrum and appendages employed by head larvae of crustaceans. The feeding nauplius evolved through evolutionary changes that began with earlier arthropod head larvae.

It appears that feeding head larvae originated very early in the evolution of bilaterians but they did not all originate in association with environmental conditions or a biota that were unique to a narrowly limited period.

Adapting front ends of animals to be most of the larval body. The minimal equipment for a larva that swims but does not feed can be developed early. Blastulae and gastrulae are capable of ciliary propulsion with passive orientation and stability (McDonald and Grünbaum 2010; McDonald 2012) and with swimming adjustedDraft in response to temperature and shear (McDonald 2004, 2012). Response to other environmental stimuli, as in habitat selection at settlement, can await further development. Feeding larvae need more equipment, and more than a functional gut.

Food for a small planktonic animal is small and scarce. A feeding larva needs to concentrate algal cells and other particulate foods before ingesting them or to detect individual food items and bring them to the mouth by other means (Hart 1991; Phillips and Pernet 1996; Bruno et al.

2012; Pernet 2018). These methods of feeding require complex equipment.

In bilaterians, the complex structures required for feeding can be developed early by employing structures at the anterior end of the animal. A differentiation of body parts that begins at the anterior and proceeds posteriorly is the likely ancestral condition for most bilaterians, and many animals add body parts in a posterior zone just anterior to the anus (Jacobs et al. 2005). A mobile animal benefits from early function of structures at its leading end. When a front end is adapted for mobility and feeding, before development of more posterior structures, the result is a head larva. A feeding larva constructed largely from anterior structures is often quite different

from later developmental stages, in which more posterior structures contribute to mobility and

feeding. One reason that larvae differ from the succeeding juvenile and adult stages is that the

larvae have fewer parts. Differences in feeding and locomotion can follow from the different

number of parts as well as from differences in size and habitat. The conditions favoring the

evolution of larval forms were developmental as well as environmental.

Anterior to posterior development appears to underlie divergence of larval and adult

forms independently in diverse bilaterians. Different anterior structures were adapted for

different mechanisms of feeding in each of several clades. In three of the clades reviewed here,

the crustaceans, brachiopods, and ambulacrarians, structures for larval feeding appear to be

modifications of structures of ancestral adult-like juveniles. The opposed band feeding mechanism of molluscan veligers and manyDraft trochophores, in contrast, depends in part on the prototroch, a band of cilia employed for swimming at early stages and not persisting beyond

early stages. The antecedent structures, whatever their nature, appear to have been anterior.

Origins of larvae as other body plans. Head larvae are “the other body plan” in several

major clades of animals (Raff 2008) because much of the eventual body has not developed.

Development of such larvae requires little of the regional anterior to posterior expression of Hox

genes that commonly accompanies development of the adult body of bilaterians (Arenas-Mena

2010; Hejnol and Vellutini 2017; Gąsiorowski and Hejnol 2019, 2020).

To frame hypotheses for origins of larvae as the two alternatives larva-first or adult-first

may mislead. Animals have changed to differing extents at different stages of development in

different lineages. A head larva is not simply an intercalation in a life history. It is a modification

of anterior development for early function.

Potential advantages of feeding head larvae in life histories. The evolution of larvae from

front ends emphasizes early development of capabilities based on fewer body parts. Animals

30 whose embryos have little protection become mobile early in development, presumably because mobility increases their survival (Ohman et al. 2002; Staver and Strathmann 2002; Bi et al.

2011). Also, initiation of feeding when there are fewer body parts enables, at the extreme, development from a smaller egg, and production of smaller offspring allows production of more offspring. Annelids with the smallest eggs are those that commence larval feeding with no or few setigerous segments (Schroeder and Hermans 1975). Similarly, among crustaceans, the smallest eggs of copepods and barnacles that first feed as nauplii are smaller than the smallest eggs of malacostracans, who commence feeding when they have additional pairs of limbs (Strathmann

2018). Development from very small eggs does not depend entirely on few pairs of limbs, however; some of the parasitic barnacles, whose first nutrition is within a host, have extremely small eggs despite developing thoracic limbsDraft as non-feeding cyprid larvae (Høeg and Lützen 1995). Also, there is extensive overlap in size of eggs of crustaceans initiating feeding as nauplii and those initiating feeding at later stages. Nevertheless, although miniaturization and rapid development to first motility or feeding depends on more than doing it with fewer body parts, advantages of developing motility and feeding early or at small size may have contributed to the origins of head larvae.

Some head larvae of early origin were swimming suspension feeders, but not all. In many extant arthropods, head larvae and adults occupy the same habitat. That may have occurred at the origin of some arthropod larval forms. The protonymphon and adults of pycnogonids are both benthic (Vilpoux and Waloszek 2003). Many protaspides of trilobites are inferred to have been benthic (Chatterton and Speyer 1997).

Limited opportunities for origins of feeding head larvae. The window of opportunity for evolution of a feeding head larva appears to have been confined to earlier stages in the radiation of bilaterians, although exceptions may possibly have occurred among animals that develop

preoral ciliary bands for early motility. Two hypotheses might account for an innovation like a

head larva being limited to the early evolution of bilaterians (Strathmann 1978b). The hypotheses

are not mutually exclusive. One is that developmental and functional constraints were acquired

with later evolutionary changes. As an example, in echinoderms postlarval stages have been

greatly modified from the presumed ancestral condition for ambulacrarians. Modification of a

head can preclude evolution of a head larva. The other is escalation among marine organisms in

what is functionally sufficient. An increase in some capabilities can restrict the origin of others.

For many animals, ancient events continue to shape available life-history trade-offs.

Having a feeding head larva, a trait that originated a half billion years ago, confers present

possibilites for increased fecundity by reduction in egg size or for earlier development of feeding. Evolutionary loss of a feeding headDraft larva can restrict those possibilities both now and in the future.

Future evolutionary prospects. If losses of a kind of larval feeding are irreversible, then

its persistence in a clade depend on differential extinction and speciation in lineages with and

without the larval feeding mechanism and on rates of evolutionary loss through transitions to

non-feeding. Such losses can occur. For example, Hansen (1982) presents fossil evidence of

decline of proportion of species with feeding veligers in several families of gastropods from the

Paleocene through the Eocene, with the Volutidae entirely without feeding larvae today.

However, traits that impose or facilitate greater larval dispersal can be correlated with lower

rates of extinction relative to speciation, as with sacoglossan gastropods with and without

feeding larvae (Krug et al. 2015) and with molgulid ascidians with and without tails (Maliska et

al. 2013). The greater dispersal associated with feeding larvae may be one feature contributing to

their persistence, although that effect of larval feeding would not apply to persistence of feeding

by benthic nauplii with little dispersal.

Another possibility is loss of all lineages with a kind of feeding larva during unusual conditions, such as a period of mass extinctions. As we change the earth’s environments, will some feeding larval forms be irreversibly lost? In so far as the mass extinction at the end

Permian and early Triassic is a model for present human environmental impacts, selective extinction of animals because of their feeding larval stage is not expected. Clearly some survivors of this extinction event had a feeding larval stage, such as gastropods, whose fossils from the Early Triassic provide no indication of selective extinction of species with feeding larvae (Nützel 2014; Nützel et al. 2018), or echinoids, which like crinoids suffered an extreme bottleneck of extinctions. Hypotheses for selective loss of feeding larvae had been suggested, however, for groups that lack feeding larvae today, such as the rhynchonelliform brachiopods and crinoids. Now for both groups, as explainedDraft above, evidence is against the mass extinction causing selective extinction of species with larval feeding. Also, there is no evidence for a selective loss of feeding larvae among gastropods and echinoids in the mass extinction at the end of the Cretaceous (Jablonski 1986; Smith and Jeffery 1998). A distinctive kind of feeding larva could be lost with extinction of a clade, but on present evidence, one would not expect selective extinctions as a result of the animals having a feeding larva.

Given evidence for unique ancient origins of several kinds of feeding larvae and, for some, the apparent irreversibility of loss of capacity to feed, the persistence of these forms during a half billion years is remarkable.

Acknowledgements

The direction of this and my other studies of larval evolution were determined by A. Richard

Palmer’s models demonstrating how advantages of larval dispersal diminished as scale of dispersal increased. This study benefited from comments from R. B. Emlet, S. H. D. Haddock, C.

S. Hickman, L. S. Hiebert, J. Hodin, J. Høeg, B. V. Holthuis, S. A. Maslakova, F. A. McAlary,

T. Miyashita, C. Nielsen, L. R. Page, G. Paulay, B. Pernet, L. M. Riddiford, B. J. Swalla, J. W.

Truman, G. von Dassow, and many others. The observations were supported by grants from NSF

(mostly Ocean Sciences), the Friday Harbor Laboratories of the University of Washington over

many years, and a grant from the Guggenheim foundation. F. I. M. Thomas and R. Collin helped

me obtain brachiopod larvae in Florida and Panama.

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Draft

Table 1. Times of origin of four kinds of feeding larvae that are indicated by fossils.

Name of larva, Taxon Origin before or by … Evidence

Nauplius, Crustacea Cambrian Stage 3, Atdabanian Body fossil of metanauplius

No name, Brachiopoda Cambrian Stage 2, Tommotian Shell form and size at umbo

Dipleurula, Ambulacraria Cambrian Stage 3, Atdabanian Adult fossils, larval

homologies and function

Veliger, Mollusca Ordovician Size of shell at apex

Note: Other inferences of homology or evidence from molecular clocks would suggest earlier

origins for some of these feeding larvae. Draft

Figure Legends

Fig. 1. Head larvae. (A) Larva and adult of a cephalocarid crustacean (ecdysozoan).

Abbreviations: a1 first antenna, a2 second antenna, m mandible. (B) Diagram of larva and metamorphosis of an enteropneust hemichordate (deuterostome). (C) Diagram of early and later stage larva of an annelid (lophotrochozoan). Larval motility and feeding commence with anterior structures before posterior body parts develop. A nauplius simplified after Sanders (1963a) and adult from Sanders 1963b. B and C from Lacalli (2005).

Fig. 2. Fossil of a crustacean metanaupliusDraft from the Early Cambrian. Labels: a1, site of first antenna; a2c, coxa of second antenna; ey, eye; hs, hypostomal spine; lab, labrum; mdb, basipod of mandible; mdc, coxa of mandible; mx1, first maxilla. The scale bar for the photo on the left is

100 µm. (From Zhang et al. 2010).

Fig. 3. Inferred evolution of nauplii: 1, initiation of motility and feeding with a small number of anterior appendages; 2, enditic spines at the base of second antenna and mandible; 3, naupliar labrum; 4, number of limb-bearing segments in first larval stage reduced from 4 to 3. Diagram simplified from Maas et al. (2003), Maas and Waloszek (2005); Zhang et al. (2012).

Fig. 4. Inferences on ancestral feeding larvae and relationships. Presence of a larval trait indicates presence in some members of a clade. Absence of a trait indicates no known occurrence in a clade. Presence of a metatroch and food groove for larval feeding, mt. Relationships simplified from Kocot et al. (2017).

Fig. 5. Feeding larvae of a discinid brachiopod at unshelled early stage (left) and shelled late

stage (right). Setae change during larval development. Labels: lo, tentacles of lophophore; se,

setae; sh, shell.

Fig. 6. Two views of the dorsal larval shell retained at the umbo of a shell of an Early Cambrian

acrotretoid brachiopod. Labels (and inferences) from earliest to latest shell growth: prms,

premetamorphic shell (the shell formed before metamorphosis, including both pr, the protegulum

(initial larval shell, formed simultaneously before subsequent growth), and bs, brephic shell

(shell added with subsequent larval growth); ha, halo (a change in shell secretion at metamorphosis); poms, post-metamorphicDraft shell (shell added after metamorphosis), including both ns, neanic shell (initial shell added after metamorphosis), and mas, mature shell (shell with

adult surface features, added after neanic shell). Scale lines 100 µm. (From Zhang et al. 2018).

Fig. 7. Diagramatic sections through ciliary bands of larvae. Brachiopoda (Lingulata) fr frontal

cilia, lf laterofrontal cilia, la lateral cilia. Ambulacraria (Ophiuroidea) cf circumoral field, cb

ciliary band. Mollusca (Gastropoda) pt prototroch, fg food groove, mt metatroch.

Fig. 8. Larvae of ambulacrarians. (A) Tornaria of an enteropneust hemichordate. (B) Binnaria of

an asteroid echinoderm. (C). Auricularia of a holothuroid echinoderm, with an example of the

path of a captured food particle, after Hart’s (1991) observation. The path before contact with the

ciliary band indicates the current for swimming and feeding. The path immediately after contact

with the ciliary band indicates the locally reversed current that is briefly induced by the food

particle, retaining it on the circumoral field and directing it toward the mouth. Asterisks indicate

58 initial and second captures at the ciliary band as the particle is conveyed to the mouth. (D)

Doliolaria of a holothuroid echinoderm. At metamorphosis swimming speed is increased by reorganization of the continuous ciliary band of the auricularia, which serves for both feeding and swimming, into a series of transverse bands of cilia in the doliolaria, solely for swimming.

Arrowheads point to transverse ciliary bands.

Draft

Fig. 1. Head larvae. (A) Larva and adult of a cephalocarid crustacean (ecdysozoan). Abbreviations: a1 first antenna, a2 second antenna, m mandible. (B) Diagram of larva and metamorphosis of an enteropneust hemichordate (deuterostome). (C) Diagram of early and later stage larva of an annelid (lophotrochozoan). Larval motility and feeding commence with anterior structures before posterior body parts develop. A nauplius simplified after Sanders (1963a) and adult from Sanders 1963b. B and C from Lacalli (2005).

182x149mm (300 x 300 DPI)

Fig. 2. Fossil of a crustacean metanauplius from the Early Cambrian. Labels: a1, site of first antenna; a2c, coxa of second antenna; ey, eye; hs, hypostomal spine; lab, labrum; mdb, basipod of mandible; mdc, coxa of mandible; mx1, first maxilla. The scale bar for the photo on the left is 100 µm. (From Zhang et al. 2010).

182x54mm (300 x 300 DPI)

Draft

86x99mm (300 x 300 DPI)

187x76mm (600 x 600 DPI) Draft

Draft

Fig. 5. Feeding larvae of a disciniscid brachiopod at unshelled early stage (left) and shelled late stage (right). Setae change during larval development. Labels: lo, tentacles of lophophore; se, setae; sh, shell. (Photos copyright R. R. Strathmann)

86x65mm (300 x 300 DPI)

Fig. 6. Two views of the dorsal larval shell retainedDraft at the umbo of a shell of an Early Cambrian acrotretoid brachiopod. Labels (and inferences) from earliest to latest shell growth: prms, premetamorphic shell (the shell formed before metamorphosis, including both pr, the protegulum (initial larval shell, formed simultaneously before subsequent growth), and bs, brephic shell (shell added with subsequent larval growth); ha, halo (a change in shell secretion at metamorphosis); poms, post-metamorphic shell (shell added after metamorphosis), including both ns, neanic shell (initial shell added after metamorphosis), and mas, mature shell (shell with adult surface features, added after neanic shell). Scale lines 100 µm. (From Zhang et al. 2018).

86x53mm (300 x 300 DPI)

Fig. 7. Diagramatic sections through ciliary bands of larvae. Brachiopoda (Lingulata) fr frontal cilia, lf laterofrontal cilia, la lateral cilia. AmbulacrariaDraft (Ophiuroidea) cf circumoral field, cb ciliary band. Mollusca (Gastropoda) pt prototroch, fg food groove, mt metatroch.

177x103mm (300 x 300 DPI)

Fig. 8. Larvae of ambulacrarians. (A) Tornaria of an enteropneust hemichordate. (B) Binnaria of an asteroid echinoderm. (C). Auricularia of a holothuroid echinoderm, with an example of the path of a captured food particle, after Hart’s (1991) observation. The path before contact with the ciliary band indicates the current for swimming and feeding. The path immediately after contact with the ciliary band indicates the locally reversed current that is briefly induced by the food particle, retaining it on the circumoral field and directing it toward the mouth. Asterisks indicate initial and second captures at the ciliary band as the particle is conveyed to the mouth. (D) Doliolaria of a holothuroid echinoderm. At metamorphosis swimming speed is increased by reorganization of the continuous ciliary band of the auricularia, which serves for both feeding and swimming, into a series of transverse bandsDraft of cilia in the doliolaria, solely for swimming. Arrowheads point to transverse ciliary bands.

182x68mm (300 x 300 DPI)