Evolution, 4th Edition

MACROEvOLuTiON: EvOLuTiON AbOvE THE SPECiES LEvEL 529

of a genetic-developmental program that had been reduced or unexpressed in the

species’ ancestors. The same phenomenon is seen in “deep homology,” a term Neil

Shubin and colleagues use to describe genetic regulatory pathways that may be

widely inherited and independently expressed in different evolving lineages, and that

may contribute to morphologically disparate features [96]. For example, homologues

of the Pax6 gene initiate the development of eyes in arthropods, vertebrates, and other

animals, and a genetic pathway governed by the Distal-less gene is the basis for many

structures (such as legs and horns) that originate in diverse

phyla as evaginations from the body wall (FIGURE 20.10).

Novel characteristics are generally thought to be based

on new regulatory interactions among previously uncon-

nected genes [10, 55], which Wagner terms character

identity networks [112]. Different states of a biologically

homologous character, then, share the same fundamental

network, together with some genes that may be included

in the network in some species but not others. A striking

example is the evolution of sex combs in the genus Drosoph-

ila [55]. These are groups of highly modified bristles on the

tarsus (foot) of male flies that are used to hold or contact

females. Species vary greatly in the number, shape, and spa-

tial arrangement of the bristles and in how they are used

(FIGURE 20.11). The development of cells into sex combs

depends on the male-specific splice form of the transcrip-

tion factor doublesex (dsx), which is expressed in parts of

the developing tarsus due to information provided by many

signal pathway genes. Within these regions, dsx and a Hox

gene called Sex combs reduced (Scr) are expressed and form a

positive feedback loop: Scr activates dsx expression, and dsx

affects the expression level of Scr. Scr is required to specify

the exact position of the sex comb and the number of teeth

(modified bristles), and dsx specifies the male-specific mor-

phology of the bristles. The expression of these genes differs

among species, and corresponds to the size and morphology

of the sex combs. These key genes regulate many down-

stream genes that determine exactly where and how the

modified bristles are formed. Thus, a new structure is based

on a novel genetic network of regulatory interactions among

several key genes, their control by upstream genes, and their

interactions with many downstream genes.

From Microevolution to

Macroevolution

Rates of evolution

The rate of evolutionary change (i.e., change per unit of

time) varies greatly among characters, among evolving lin-

eages, and within the same lineage over time. In general,

the longer the time interval over which rates of evolution

are measured, the lower the rates are, because when the

interval is long, many short periods of rapid and reversing

evolution are averaged into a much slower net rate of evo-

lution (FIGURE 20.12A). Many characteristics have been

seen to evolve very rapidly in living populations, in which

Futuyma Kirkpatrick Evolution, 4e

Sinauer Associates

Troutt Visual Services

Evolution4e_20.11.ai Date 12-27-2016

Ancestral pathway New sex-specic pathway

subgenus

Drosophila

Spatial cues

Scr

dsx

Bristle

patterning

Spatial cues

Scr

dsx

Bristle

patterning

Tissue rotation

Sex-specic bristle pattern

Bristle shaft morphogenesis

Melanogaster +

obscura clade

D. cusphila D. biarmipes

FIGURE 20.11 A model of evolutionary change in gene interac-

tions that underlie the differentiation of specific bristles into sex

combs in the melanogaster + obscura clade of Drosophila. The

photos are from two species that are related to D. melanogaster.

The left-hand image in each pair of photos shows transverse sex

combs on the tarsal segments; the right-hand image in each pair,

without sex combs, shows developing segments in which the

distribution of the Scr protein, detected by antibody staining,

is indicated by the dark areas. In the diagram of phylogenetic

history, ancestral regulatory interactions are indicated in black,

and new interactions in red. Ancestrally, drosophilid flies lack sex

combs; Scr is expressed in specific parts of the developing tarsus,

and organizes the development of the same bristle pattern in

both sexes. In the melanogaster + obscura clade, interaction of

Scr with dsx results in male-specific differentiation, and both dsx

and Scr regulate downstream genes involved in the processes

listed. (After [55]; photos courtesy of Artyom Kopp.)

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