Evolutionary Relationships of the Arthropoda I

1.  Trilobitomorpha (extinct) — trilobites

2.  Chelicerata — horseshoe crabs, spiders, scorpions, ticks, mites, solifugids

3.  Crustacea—brine shrimp, barnacles, fish lice, lobsters, crabs and shrimp

4.  Myriapoda — centipedes, millipedes

5.  Hexapoda — insects, entognathans

Insects are a class (Insecta) in the phylum Arthropoda The Arthropoda is the largest phylum of organisms and accounts for over 75% of all species on Earth. Major groups (subphyla) within the Arthropoda are:

Representative Arthropods

Trilobitomorpha

Crustacea

Myriapoda

Chelicerata

Hexapoda

Major Characteristics of the Arthropoda •  External and internal body seg-

mentation with regional specialization (tagmosis).

•  Paired articulated (jointed) appendages surrounded by chitinous cuticle. Arthropoda means jointed (arthro) leg (poda).

•  Cuticle forms a well developed exoskeleton, generally with thick sclerotized plates.

•  Paired compound eyes usually present (sometimes lost secondarily).

•  Growth by the process of ecdysis (molting).

•  Coelom reduced to portions of the reproductive and excretory systems.

•  Muscles are striated and arranged in isolated, segmental bands.

Three major questions regarding the evolutionary relationships of the Arthropoda

1. How are arthropods related to other major phyla of invertebrates, particularly the Annelida (segmented worms) and the Mollusca (snails, bivalves, octopus and squid)?

2. Are arthropods a single evolutionary lineage, or have the characteristics that unite them evolved multiple times?

3. What is the evolutionary relationship of insects to the other major groups (subphyla) in the Arthropoda?

To answer these questions we need to review some terms and concepts used in analyzing evolutionary relationships. In particular, we need to define what we mean by an evolutionary relationship, what kind of data we use to determine evolutionary relationships, and how we represent these evolutionary relationships.

Three Kinds of Phylogenetic Relationships •  Monophyletic. A group of species that

includes an ancestral species and all of its descendants. These species comprise a single evolutionary lineage and share a unique history of descent. Monophyletic groups are called “natural” because they represent the “true” evolutionary history of the groups.

•  Paraphyletic. A group in which member species are all descendent from a common ancestor, but which does not contain all the species descended from that ancestor. Class Reptilia (turtles, snakes, lizards and crocodilians) in the vertebrates is a good example of a paraphyletic group because it excludes birds, which is the sister group of the crocodilians.

•  Polyphyletic. A group in which member species share more than one immediate ancestor. Polyphyletic groups are “artificial” because they do not shared a common immediate ancestor. They occur when convergent or non-homologous characters are used to define or diagnose a group. Endothermic vertebrates is an example of a polyphyletic group because birds and mammals do not share an immediate common ancestor.

Characters Used in Phylogenetic Analysis •  Homologous characters are features that have

the same evolutionary origin as determined by positional, developmental and genetic studies. Only homologous characters are useful in recovering the evolutionary history of a group of taxa.

•  Convergent (analogous) characters are features that perform similar functions, but have different evolutionary origins. Convergent characters cannot be used to reconstruct evolutionary history, but they are very useful in comparative studies of performance (e.g., insect versus vertebrate flight).

Fossorial forelegs in five different genera

Homologizing structures in the heads of stalk-eyed flies in two different families

Two Kinds of Similarities in Homologous Characters

•  Apomorphies are characters that arose in a most recent common ancestor, or a recently evolved (“advanced”) feature that appears only in a group of closely related species. Apomorphies that are unique to a particular taxon are called autapomorphies. Autapomorphies are useful in identifying a taxon and distinguishing it from other groups (a diagnostic trait). Apomorphies that are shared among taxa are called synapomorphies.

•  Plesiomorphies are characters that arose in a distant common ancestor, or “primitive” features that are shared by distantly related species. Plesiomorphic characters that are shared between two or more taxa are called symplesiomorphies.

•  Determining which characters are apomorphic and which are pleisomorphic is accomplished by a character polarity analysis. Examination of character distribution in groups known to be basal relative to the one under study is one popular way to polarize characters (outgroup comparison). Traits shared between the outgroup and the ingroup are plesiomorphies, whereas those share within the ingroup are apomorphies.

•  Plesiomorphy and apomorphy are relative terms. Each homologous character is a synapomorphy at only one level of a phylogeny and is a sympleisomorphy at a deeper level of the phylogeny. For example, wings are a plesiomorphy of butterflies because they are shared with butterflies (ingroup) and with their closest relatives (outgroup). Wings are an apomorphy of pterogyotes (winged insects) because they are not shared with pterogyotes and their closest relatives (Thysanurans).

•  Taxa based on apomorphies are monophyletic, whereas taxa based

on plesiomorphies are paraphyletic.

Lepi

dopt

era

Tric

hopt

era

Oth

er N

eopt

era

Thys

anur

a

Oth

er P

tery

gota

Oth

er A

pter

ygot

a

Wingless

Winged

Phylogenetic Analysis •  Evolutionary trees are constructed by analyzing the

topological arrangement of the homologous traits (apomorphies and plesiomorphies) identified in the taxa under study (ingroup) in comparison with the outgroup.

•  A cladogram is a graphic representation of the origins of synapomorphies. In its ideal form a cladogram depicts a completely nested set of synapomorphies. A cladogram is a very general evolutionary tree that indicates only relative relationships and not the timing evolutionary events. A phylogeny is a cladogram calibrated with the fossil record and the geological time scale.

•  Each split or dichotomy in the cladogram produces a pair of newly derived taxa that are called sister-taxa or sister-groups.

•  The more synapomorphies that are nested in a consistent manner, the higher the level of congruence for the cladogram. However, not all cladograms show a completely consistent nested set of synamorphies. Low levels of congruence may be due to mistakes in determining which characters are homologous and which are homoplastic, or the result of evolutionary convergence. Low levels of congruence may also result from mistakes in determining which characters are plesiomorphic and which are apomorphic.

Lepi

dopt

era

Tric

hopt

era

Oth

er N

eopt

era

Thys

anur

a

Oth

er P

tery

gota

Oth

er A

pter

ygot

a

Wings covered in scales

Wings present

Wings covered

Wings folded

Dicondylic mandibles

Major Branches in Animal Phylogeny

Protostomes

Deuterostomes

Ctenophores

Echinoderms Sea Squirts Lancets Vertebrates Molluscs Annelids Rotifers Flatworms Nematodes Tardigrades Onychophorans Arthropods

Porifera Cnidaria

Bilateral

Radial

Radial

Multicellular Ancestor

Characteristics of Phylum Annelida • Annelids (from Latin annellus

for “little ring”) are the segmented worms the include earthworms, marine worms (polychaetes) and leeches. There are about 15,000 species worldwide.

• Characteristics shared with the Arthropoda include serial arranged body segmentation (metamerism), double ventral nerve cord, dorsal and ventral longitudinal muscles, and a dorsal blood vessel with forward-going peristalsis.

Characteristics of the Mollusca

• Molluscs (from Latin molluscus for “soft”) include the gastropods (snails and slugs), bivalves (clams and mussels) and the cephalopods (squids and octopus). There are about 93,000 species worldwide.

• Characteristics shared with the Annelida include pelagic larvae (trochophore) with one or more bands of locomotory cilia located equatorially (near the mouth) and formed before gastrulation, pelagic larva with para- or circumanal ciliary tuft, and paired excretory organs and ducts that open externally (nephridiopores).

Apical tuft (cilia)

Prototroch (cilia) Stomach

Mouth

Anus

Metatroch (cilia) Mesoderm

Trochophore larva

Relationship of Arthropoda to Other Phyla •  Hypothesis 1. Arthropoda is the sister group of

the Annelida, which together comprise the Articulata. Mollusca is the sister group of the Articulata.

•  Hypothesis 2. Annelida and Mollusca are sister groups, which together comprise the Eutrochozoa. Arthropoda is the sister group of the Eutrochozoa.

•  Hypothesis 3. Arthropoda and Mollusca are sister groups and Annelida is the sister group of the Arthropoda + Mollusca clade.

•  These 3 phylogenetic hypotheses can be “tested” by mapping apomorphic characters on to cladograms and counting up the number of steps required. By the principle of parsimony, the hypothesis with the least number of steps is more likely to be true.

•  Parsimony analysis provides equal support for hypothesis 1 (Articulata) and hypothesis 2 (Eutrochozoa). In each instance, a minimum of three evolutionary changes are required. Hypothesis 3 requires at least four evolutionary changes and is therefore less parsimonous.

Most Recent Phylogeny for Protostomes •  Recent phylogenetic analysis based on

molecular characters (Dunn et al 2008) suggest two major lineages within the Protostoma: 1) the Lophotrochozoa, which include the molluscs, the annelids several other phyla, and 2) the Ecdysozoa, which include the Arthropoda, Onychophora, Tardigrada and Nematoda.

•  The lophotrochozans are split into two groups those that have lophophores, a fan of ciliated tentacles surrounding the mouth (bryozoans, brachiopods, ectoprocts, and phoronids) and those that have trochophore larvae (molluscs and annelids, and several other worm-like groups). There is debate on whether these subgroups are monophyletic, or even whether the lophophorates are protostomes!

•  The ecdysozoans all share a three-layered cuticle composed of organic material, which is periodically molted as the animal grows, hence the name. There is still controversy over whether this group is monophyletic and some researchers still place the annelids as the sister group to the arthropods or the panarthropods (arthropods + onychophorans).

Alternative Phylogeny for the Ecdysozoa

•  One problem with the previous phylogeny of the protostomes is that it places the tardigrades as the sister group to the nematodes, which complicates our understanding of the evolution of segmentation and other characters associated with arthropods (paired limbs with claws).

•  Telford et al. (2008) proposed an alternative phylogeny of the Ecdysozoa which places the tardigrades + onychophorans as the sister group to the Arthropods (Eurarthropods).

•  Note there are other differences between the Dunn et al and the Telford et al phylogenies, including the placement of the Myriapoda. We’ll cover that topic in the next lecture.

Conclusions •  We answered the first of our three questions regarding the

phylogenetic relationships of the Arthropoda, at least tenetatively. Molluscs and annelids are more closely related to each other than either is to arthropods. This means that segmentation as observed in arthropods and annelids is homoplastic and not homologous. In contrast, the trochophore larvae present in molluscs and annelids is probably a true homology.

•  We also learned that having more characters in a phylogenetic analysis does not necessarily make things easier. More characters may mean more chances for conflicts in terms of the hierarchical nesting of them. Molecular characters may improve phylogenetic analysis, but errors may occur when the rates of evolution are vastly different in different lineages (e.g., the long branch attraction problem, a problem seen in nematodes).

•  We will address our other two questions in the next couple of lectures when we examine the phylogenetic relationships within the Arthropoda and the relationships of insects to the other groups.