Development and Evolution

1. Development and Evolution Chapter 18

2. “A great deal of the problem of neo-Darwinian theory is that it is strictly a theory of genes, yet the phenomenon that has to be explained in evolution is that of the transmutation of form. True, genes may be invented to account for the selection of any desired form, but the real solution to the problem lies in that uncharted realm between genes and morphology.”M. W. Ho and P. T. Saunders. 1979. Beyond neo-Darwinism — an epigenetic approach to evolution. J. Theoretical Biology 78:573-591.

3. The morphologists’ complaint • The modern synthesis, which has dominated much evolutionary thinking since the mid-20th Century, is a synthesis of Darwinian verbal argument and mathematic population genetics – it seeks to explain evolutionary change ultimately in terms of forces acting to change allele and genotype frequencies in populations • Population genetics thinking does not, and cannot, explain much of what is interesting about evolution – particularly the evolution of morphology of multicellular animals

4. Morphology is epigenetic • Morphology results from interaction between many gene products and between gene products and the environment and is expressed only through development ( = ontogeny) • We can’t understand the evolution of morphology simply by reference to forces that change allele and genotype frequencies in populations, or simply by understanding how a sequence of DNA nucleotides specifies a sequence of amino acids

5. “Evo-Devo” • Animal body plans • Formation of limbs in vertebrates and arthropods • Evolution of the flower

6. Homeotic genes and pattern formation • Homeotic loci are genes that are responsible for telling cells where they are spatially in a developing 4 -dimensional embryo, for telling cells where they are in a developmental sequence, and for determining the fates of cells • In animals, the key homeotic loci are called Hox (for “homeobox”) or HOM genes – they are a gene family created by gene duplication events • In plants, the key homeotic genes are the MADS-box genes • Although there are Hox homologues in plants and MADS-box homologues in animals, Hox loci and MADS-box loci are not homologous to each other

7. Hox genes in animals • Found in all major animal phyla • Occur in groups (gene duplication events) – the number of genes in each group and the total number of groups varies among phyla • Perfect correlation between the 3’ – 5’ order of genes along the chromosome and the anterior to posterior location of gene products in the embryo. Genes at the 3’ end are also expressed earlier in development and in higher quantity than genes at the 5’ end – spatial, temporal, and quantitative colinearity • Each locus within the complex contains a highly conserved 180 bp sequence, the homeobox, that codes for a DNA binding motif – Hox gene products are regulatory proteins that bind to DNA and control the transcription of other genes

8. Hox genes in Drosophila • Two clusters – Antennapedia and bithorax • Mutations in the Antennapedia genes affect the anterior of the developing embryo, mutations in bithorax genes affect the posterior • Flies missing one or more Hox gene products produce segment-specific appendages such as legs or antennae in the wrong place • Gene products from Hox loci demarcate relative positions in the embryo, rather than coding for specific structures – for example, they specify “this is thoracic segment 2” rather than “make wing”

9. Hox genes in Drosophila(Gerhart and Kirschner 1997) (Fig. 18.1)

10. Hox gene mutant phenotypes • Top: normal fly on left; antennapedia mutant phenotype on right • Bottom: bithorax mutant phenotype

11. The phylogenetic position of Hox genes • Although Hox genes are expressed in a segment-specific way in arthropods, they are also found in non-segmented animals – they are not “segmentation genes” • Hox genes specify anterior – posterior and dorso – ventral axes in bilateral animals, but homologues are present in sponges and jellyfish, and plants and fungi • The original gene duplication event that produced the Hox complex may have preceded the evolution of multicellularity in animals • 10 Hox loci probably existed in the common ancestor of all bilaterally symmetric animals – sponges and cnidarians have just 3 – 4 Hox loci • There is a rough correlation between the number of homeotic loci and complexity of metazoan body plans • Vertebrates have 4 Hox clusters, but other deuterostomes have just a single cluster

12. Hox genes in various animal phyla (Fig. 18.3)

13. Changes in Hox expression: arthropod segmentation • Does variation in Hox gene expression correlate with morphological diversity in arthropods? • All arthropods (+ onychophorans) have the same 9 Hox genes • Addition of sequences coding for an alanine region in the product of Ubx may be responsible for the suppression of legs on the abdominal segments of insects

14. Hox expression and arthropod segmentation (Knoll and Carroll 1999) (Fig. 18.5)

15. The origin of the tetrapod limb • Phylogenetic and morphological analyses support the hypothesis that the tetrapod limb is derived from the fins of lobe-finned fish • The first tetrapods (amphibians) appear in the late Devonian, about 365 mya

16. Lobe-finned fish and the tetrapod limb (Figs. 18.6 and 18.7) • Eusthenopteron, a lobe-finned fish from the Devonian (409-354 mya)

17. The developing tetrapod limb budAER = apical ectodermal ridge (Fig. 18.8)

18. The development of the tetrapod limb -1 • The tip of a growing limb bud is the apical ectodermal ridge (AER) – cells in the AER secrete a substance that keeps the underlying cells in a growing and undifferentiated state (the progress zone) – this determines the long axis of the limb • The zone of polarizing activity (ZPA) is formed by a group of cells at the base of the limb bud – these cells secrete a substance that forms a gradient in the surrounding tissue and gives cells in the limb bud positional information

19. The development of the tetrapod limb -2 • The substance secreted by cells in the AER is the product of the gene fibroblast growth factor 2 (FGF-2) – this determines the proximal - distal axis of the limb • The substance secreted by cells in the ZPA is the product of a gene called sonic hedgehog (shh) – this determines the anterior - posterior axis of the limb • Expression of a gene called Wnt7a is responsible for determining the dorso - ventral axis (wingless + int-1) • Hox genes are also expressed in the tetrapod limb and may tell cells where they are along the length of the limb

20. The development of the tetrapod limb -3 • One implication of this line of research is that evolution of limb morphology in tetrapods may result from changes in the timing or level of expression of the pattern forming genes – Fgf-2, shh, Wnt, or the Hox genes • Evolution of the hand and foot (not present in lobe-finned fish) may be due in part to turning expression of shh and Hox genes back on in the late limb bud of tetrapods

21. Arthropod limbs (Brusca and Brusca 2002) (Fig. 18.12) • Uniramous • Biramous

22. Genetic control of limb formation in arthropods • The decision whether to make a limb depends on a gene called wingless (wg) • Wingless is expressed in the anterior of limb primordia and another gene, engrailed (en), is expressed in the posterior – these two genes appear to determine the anterior - posterior axis of the limb • The decision to extend the limb distally appears to be due to the expression of the gene Distal-less (Dll) – this is the first gene activated specifically in limb primordia • The decision on which type of limb will develop is controlled by Hox genes • Variation in the timing and location of expression of Distal-less appear to affect the branching pattern of arthropod limbs

23. Deep Homology • Distal-less has been found to play a role in limb formation in all bilaterians examined to date – arthropods, vertebrates (cells of the AER), onychophorans, annelids (parapodia), echinoderms (tube feet) • Furthermore, it is also known that similar genes in mice and fruit flies are involved in the formation of eyes, hearts, nerve cords, and segmentation

24. MADS-box homeotic genes and development of flowers • Specify which floral organs appear where • Each locus encodes a DNA binding protein domain (MADS box) that is analogous to the DNA binding domain encoded by Hox genes • Mutations in specific MADS-box genes are associated with abnormal floral morphology

25. Parts of a flower (Fig. 18.15)

26. The ABCs of flower development mutations(Coen 1999) (Fig. 18.16) APETALA1 mutation APETALA3 mutation AGAMOUS mutation

27. A conceptual model of flower formation by homeotic genes (Parcy et al. 1998) (Fig. 18.18)

28. Genes and development – summary • The evo-devo research program of the last 20 years has done much to answer the criticisms of the modern synthesis that were made by developmental biologists and morphologists in the early 1980’s • We are now beginning to understand the genes and gene interactions that are responsible for the development and evolution of complex body plans and morphology in animals, and floral structures in plants • Macroevolutionary change in morphology can be understood in terms of changes in a set of genes common to all animals (or plants) – deep homology – and that are affected by microevolutionary processes – selection, drift, mutation, gene duplication