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Speciation: Genital divergence and the evolution of reproductive isolation

Speciation and diversity in genitalia

Speciation requires reproductive isolation and biologists have examined multiple different processes of lineage splitting by which it could evolve. Within this range, reinforcement is recognised as having a special position as the only process in which natural selection directly favours an increase in reproductive isolation. Reinforcement is an evolutionary process by which natural selection increases reproductive isolation to avoid maladaptive hybridization. Similarly, a role for genital form influencing copulatory and post-copulatory components of reproductive isolation has long been suspected because, among animals with internal fertilization, male genitalia demonstrate rapid divergent evolution and species-specific forms. However, reinforcement and genital form have virtually always been studied separately.

In the marine gastropod family Littorinidae, the form of the elaborate penis is often species specific, which has lead to speculation about its role in pre-copulatory recognition. The molecular phylogeny, taxonomy, geographical distributions and ages of divergence of this worldwide clade are known in detail. With a combination of comparative analysis, behaviour experiments and molecular techniques, this project examines speciation by reinforcement in this large phylogeny, in the context of evolution of genital form.

Figure speciation

Littoraria cingulata and L. filosa

We use Littoraria cingulata/filosa, a sister species pair that occurs predominantly on mangrove trees and reproduces by spawning pelagic larvae with wide dispersal. L. cingulata is endemic to Western Australia while L. filosa is found mainly in North and East Australia. There is a small region of overlap near Broome, which is the northern part of western Australia. In sympatry the species reside on the same trees, but occupy different vertical levels. Hybrids are sporadically discovered. This species pair provides an excellent contrast with L. fabalis/obtusata because of the far greater dispersal distance.

Littoraria

Littorina fabalis and L. obtusata

Littorina fabalis and L. obtusata are two sister species in the phylogeny of Littorinidae that show remarkable intraspecific variation in male genital form. L. fabalis also contains ecotypes adapted to different environments. In Europe, L. fabalis/obtusata are broadly sympatric from Spain up to the North Sea and Iceland, although in Portugal both allopatric and sympatric localities are known and throughout the range the proportions of the two species vary between sites and they are often partially separated by tidal level. Along the Atlantic North-American coast, L. obtusata exists allopatrically – and along the west-coast of Greenland, populations of L. fabalis/obtusata occur in both sympatry and allopatry. The two species are viviparous, laying egg-masses attached mostly to fucoid algae from which juveniles hatch. Accordingly, dispersal rate is very low among juveniles and adults.

In a recent study from Portugal shows that populations of L. fabalis/obtusata from northern Europe share significantly more mtDNA haplotypes compared to populations from Iberia, which does not support the idea of incomplete lineage sorting. Lab experiments in Sweden and in Spain confirm that the two species mate heterospecifically and can produce hybrids. Very recent microsatellite studies now support hybridization (detecting both F1 and F2) and provide evidence of nuclear introgression. There are strong signs that hybrid snails having lower fitness compared to pure parental offspring as the hybrids are born with low vigor and always die in the lab

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Johan Hollander

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Johan Hollander

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