Evolution of mating isolation between populations ofDrosophila ananassae

Abstract

Prezygotic mating isolation has been a major interest of evolutionary biologists during the past several decades because it is likely to represent one of the first stages in the transition from populations to species. Mate discrimination is one of the most commonly measured forms of prezygotic isolation and appears to be relatively common among closely related species. In some cases, it has been used as a measure to distinguish populations from subspecies, races, and sister species, yet the influences of various evolutionary mechanisms that may generate mate discrimination are largely unknown. In this study, we measured the level and pattern of mate discrimination among 18 populations of a cosmopolitan drosophilid species, Drosophila ananassae, from throughout its geographical range and its sister species, Drosophila pallidosa, which has a restricted geographical distribution in the South Pacific Islands. In addition, we measured genetic differentiation between all 18 populations using mitochondrial DNA polymorphism data. Mate discrimination varies considerably throughout the species range, being higher among populations outside the ancestral Indonesian range, and highest in the South Pacific. Our results suggest that colonization and genetic differentiation may have an influence on the evolutionary origin of mate discrimination. Our phylogeographical approach clarifies the ancestral relationships of several populations from the South Pacific that show particularly strong mate discrimination and suggests that they may be in the early stages of speciation. Furthermore, both the genetic and behavioral results cast doubt on the status of D. pallidosa as a good species.

Population genetics ofDrosophila ananassae

“…It exists in highly structured populations in Asia and South Pacific (Johnson, 1971 ;Stephan, 1989 ;Stephan & Langely, 1989;Tomimura et al, 1993 ;Stephan et al, 1998;Vogl et al, 2003 ;Das et al, 2004;Schug et al, 2007Schug et al, , 2008 and its biogeographical history is well characterized. Other peculiar characteristics are the existence of spontaneous crossing-over in males, which is meiotic in origin (Kikkawa, 1937;Moriwaki, 1937Moriwaki, , 1940Moriwaki et al, 1970;Moriwaki & Tobari, 1973 ;Matsuda et al, 1983 ;Kale, 1969 ;Hinton, 1970; ; presence of chromosome rearrangements, such as, pericentric inversions, translocations, transpositions, deficiencies and extrabands, reflecting high mutability in D. ananassae (Kikkawa, 1938).…”

Origin of sexual isolation in Drosophila ananassae due to founder effects

“…Earlier studies have shown that there is instability of mate recognition system in D. ananassae (Singh and Chatterjee 1985;Nanda and Singh 2011a, b). Schug et al (2008) have found that mate discrimination varies considerably throughout the species range being higher among the populations outside the ancestral Indonesian range and highest in South Pacific and their results suggest that colonization and genetic differentiation affect the evolutionary origin of mate discrimination of D. ananassae. The origin of premating isolating barriers among recently diverged populations is often an early step in the process of speciation (Dobzhansky 1937; Coyne and Orr 2004).…”

“…In the genus Drosophila, the phenomenon of sexual isolation (both intraspecific and interspecific) has been extensively studied and found to be widespread (Ehrman and Parsons 1980;Henderson and Lambert 1982;Speith and Ringo 1983;Hollocher et al 1997;Ting et al 2001;Haerty et al 2005;Castrezana and Markow, 2008;Schug et al 2008;Yukilevich and True 2008;Singh 2010a). There are certain studies in Drosophila which show that sexual isolation between closely related species is stronger between sympatric rather than allopatric populations.…”

Effect of chromosome arrangements on mate recognition system leading to behavioral isolation in Drosophila ananassae

“…Henderson and Lambert (1982) suggested that there is considerable stability in the mate recognition system of widely separated populations of D. melanogaster in spite of the substantial genetical and morphological differentiation that exists throughout the cosmopolitan distribution of this species. In D. ananassae, mate discrimination varies considerably throughout the species range, being higher among the populations outside the ancestral Indonesian range and highest in the South Pacific (Schug et al 2008).…”

“…In the genus Drosophila, the phenomenon of sexual isolation (both intraspecific and interspecific) has been extensively studied and found to be widespread (Ehrman and Parsons 1980;Henderson and Lambert 1982;Speith and Ringo 1983;Hollocher et al 1997;Singh 1997;Ting et al 2001;Haerty et al 2005;Castrezana and Markow 2008;Schug et al 2008;Yukilevich and True 2008). There are certain studies in Drosophila which show that sexual isolation between closely related species is stronger between sympatric rather than allopatric populations.…”