A low‐latitude species pump: Peripheral isolation, parapatric speciation and mating‐system evolution converge in a marine radiation

Abstract

Geologically recent radiations can shed light on speciation processes, but incomplete lineage sorting and introgressive gene flow render accurate evolutionary reconstruction and interpretation challenging. Independently evolving metapopulations of low dispersal taxa may provide an additional level of phylogeographic information, given sufficiently broad sampling and genome‐wide sequencing. Evolution in the marine brown algal genus Fucus in the south‐eastern North Atlantic was shaped by Quaternary climate‐driven range shifts. Over this timescale, divergence and speciation occurred against a background of expansion‐contraction cycles from multiple refugia, together with mating‐system shifts from outcrossing (dioecy) to selfing hermaphroditism. We tested the hypothesis that peripheral isolation of range edge (dioecious) F. vesiculosus led to parapatric speciation and radiation of hermaphrodite lineages. Species tree methods using 876 single‐copy nuclear genes and extensive geographic coverage produced conflicting topologies with respect to geographic clades of F. vesiculosus. All methods, however, revealed a new and early diverging hermaphrodite species, Fucus macroguiryi sp. nov. Both the multispecies coalescent and polymorphism‐aware models (in contrast to concatenation) support sequential paraphyly in F. vesiculosus resulting from distinct evolutionary processes. Our results support (1) peripheral isolation of the southern F. vesiculosus clade prior to parapatric speciation and radiation of hermaphrodite lineages‐a “low‐latitude species pump”. (2) Directional introgressive gene flow into F. vesiculosus around the present‐day secondary contact zone (sympatric‐allopatric boundary) between dioecious/hermaphrodite lineages as hermaphrodites expanded northwards, supported by concordance analysis and statistical tests of introgression. (3) Species boundaries in the extensive sympatric range are probably maintained by reproductive system (selfing in hermaphrodites) and reinforcement.

A shift in the host web occupancy of dew-drop spiders associated with genetic divergence in the Southwest Pacific

“…It is also worth noting that the AAL shows a lack of genetic differentiation over some of the very deep channels of Sulawesi and associated islands, further suggesting that deep channels are not an effective barrier to dispersal and range expansion in this organism. Similarly, our RASP results inferred an ancestral range of AOL and AAL as Taiwan, Philippines, Okinawa, Miyako and Yaeyama (DG: 37.03%); accordingly, dispersal is supported as the likely predominant process responsible for range expansion, involving faunal exchange from the ancestral range of A. bonadea to distant island populations, after which subsequent differentiation may have occurred as a function of geographical isolation (Mayr,1963; Almieda et al, 2022).…”

A shift in the host web occupancy of dew‐drop spiders associated with genetic divergence in the Southwest Pacific

“…This interpretation suggests that successful colonization was accomplished even in the presence of the Kerama Gap like in the case of the harvestman Zepedanulus ishikawai (Kumekawa et al, 2021), thus supporting overwater dispersal as a viable process underlying our inference of a structured geographical pattern. From our time-calibrated inference of historical dispersal across the Kerama Gap, we conclude that this often-cited geographical bar- Following dispersal in Okinawa, that dispersal event also occurred in Taiwan, the Philippines, Okinawa, Miyako, Yeayama, and Australia; accordingly, dispersal is supported as the likely predominant process responsible for range expansion, involving faunal exchange from the ancestral range of A. bonadea to distant island populations, after which subsequent differentiation may have occurred as a function of geographical isolation (Almeida et al, 2022;Mayr, 1963).…”

“…Similarly, our RASP results inferred an ancestral range of AOL and AAL as Okinawa (D: 52.63%). Following dispersal in Okinawa, that dispersal event also occurred in Taiwan, the Philippines, Okinawa, Miyako, Yeayama, and Australia; accordingly, dispersal is supported as the likely predominant process responsible for range expansion, involving faunal exchange from the ancestral range of A. bonadea to distant island populations, after which subsequent differentiation may have occurred as a function of geographical isolation (Almeida et al., 2022; Mayr, 1963).…”