The disruption of habitat isolation among threeHexagrammosspecies by artificial habitat alterations that create mosaic‐habitat

Abstract

In coastal areas in Japan, three species of greenling (Hexagrammos spp.) can hybridize. In a natural reef setting we showed that Hexagrammos agrammus and H. octogrammus established their breeding territories in a shallow area where seaweed was abundant, whereas H. otakii established breeding territories in a deep area that was sparsely covered with seaweed. This difference in habitat use resulted in H. otakii being distributed separately from the other two species, thereby reducing the potential for hybridization. However, all the three species co-occurred in an artificial area near a breakwater. This area is characterized by steep slopes and complex stacked concrete structures, which create a mosaic-habitat consisting of a shallow environment with seaweed and a deep environment with sparse seaweed, allowing the three species to breed within a single area. Our results suggest that man-made structures can create an artificial mosaic-habitat that can disrupt habitat isolation and promote hybridization between species.

Origins of two hemiclonal hybrids among three Hexagrammos species (Teleostei: Hexagrammidae): genetic diversification through host switching

“…Because both hybridogenetic hybrids ( Hoc / Hot and Hoc / Hag ) had Hoc mtDNA haplotypes, H. octogrammus ( Hoc ) is considered to be the maternal ancestor of these hybrids (Crow et al., ; Kimura et al., ). Although morphological (Shinohara, ) and molecular studies (Crow et al., ) have demonstrated that H. agrammus ( Hag ) and H. otakii ( Hot ) are the closest relatives (sister species), hybrids between these two species have rarely ever been observed in areas where these species are sympatrically distributed (Crow et al., ; Kimura & Munehara, ; Kimura & Munehara, ). Conversely, natural hybrids ( Hoc / Hot and Hoc / Hag ) between distant species have been shown to propagate by hemiclonal reproduction, with hybridization occurring after secondary contact (Kimura‐Kawaguchi et al., ).…”

“…However, Hexagrammos hybrids are widespread in the North Pacific Ocean, and both paternal species ( Hag and Hot ) coexist. Thus, while pre‐reproductive isolation between the paternal species of this genus is likely to have occurred due to subtle differences in habitat preference and parental care (Kimura & Munehara, , ), breeding season and site preference are known to overlap among Hag , Hot , and Hoc (Munehara, Takenaka, & Takenaka, ). For example, Hoc and Hag inhabit shallow seaweed beds, while Hot inhabits deeper reefs and sandy bottomed environments where seaweeds are scarce (Kimura & Munehara, , ).…”

“…Thus, while pre‐reproductive isolation between the paternal species of this genus is likely to have occurred due to subtle differences in habitat preference and parental care (Kimura & Munehara, , ), breeding season and site preference are known to overlap among Hag , Hot , and Hoc (Munehara, Takenaka, & Takenaka, ). For example, Hoc and Hag inhabit shallow seaweed beds, while Hot inhabits deeper reefs and sandy bottomed environments where seaweeds are scarce (Kimura & Munehara, , ). Hexagrammos species employ breeding territories and the polyandrous females visit the multiple males' territories where they spawn and produce adhesive egg masses that are then guarded by the males (Munehara, Kanamoto, & Miura, ; Munehara, Takenaka, et al., ).…”

“…Because hybrids typically have low fitness and survivability, parental species typically avoid hybridization by reinforcing species recognition, as failure to do so would result in these species interbreeding and forming a single species (Coyne & Orr, 2004;Ellstrand et al, 2010). Hemiclonal reproduction is one mechanism that allows hybrids to survive while avoiding genetic recombination (Burt & Trivers, 2006 (Kimura & Munehara, 2010, 2011. Hexagrammos species employ breeding territories and the polyandrous females visit the multiple males' territories where they spawn and produce adhesive egg masses that are then guarded by the males (Munehara, Kanamoto, & Miura, 2000;Munehara, Takenaka, et al, 2000).…”

Population genetic structure of the messmate pipefish Corythoichthys haematopterus in the northwest pacific: evidence for a cryptic species

“…For instance, three species of greenlings ( Hexagrammos agrammus , H. octogrammus , and H. otakii ), which are reproductively isolated from each other in their natural habitat because of differences in depth and spawning substrate (e.g. seaweed or bryozoans) preferences, can hybridize in artificial environments consisting of steep slopes of complexly stacked concrete structures near a breakwater (Munehara et al 2000; Kimura and Munehara 2010). Such an artificial environment would create a mosaic-habitat consisting of shallow and deep environments with diverse spawning substrate types, and consequently, increase sympatric greenling encounters.…”