Morphological, genotypic and metabolomic signatures confirm interfamilial hybridization between the ubiquitous kelps Macrocystis (Arthrothamnaceae) and Lessonia (Lessoniaceae)

Abstract

Macrocystis pyrifera and Lessonia spicata are economically and ecologically relevant brown seaweeds that recently have been classified as members of two separated families within Laminariales (kelps). Here we describe for the first time the Macrocystis pyrifera x Lessonia spicata hybridization in the wild (Chiloe Island, Southeastern Pacific), where populations of the two parents exist sympatrically. Externally, this hybrid exhibited typical features of its parents M. pyrifera (cylindrical and flexible distal stipes, serrate frond margins and presence of sporophylls) and L. spicata (rigid and flat main stipe and first bifurcation), as well as intermediate features between them (thick unfused haptera in the holdfast). Histological sections revealed the prevalence of mucilage ducts within stipes and fronds (absent in Lessonia) and fully developed unilocular sporangia in the sporophylls. Molecular analyses confirmed the presence of the two parental genotypes for ITS1 nrDNA and the M. pyrifera genotype for two predominantly maternally inherited cytoplasmic markers (COI and rbcLS spacer) in the tissue of the hybrid. A metabolome-wide approach revealed that this hybrid is more chemically reminiscent to M. pyrifera. Nevertheless, several hits were identified as Lessonia exclusive or more remarkably, not present in any of the parent. Meiospores developed into apparently fertile gametophytes, which gave rise to F1 sporophytes that reached several millimeters before suddenly dying. In-vitro reciprocal crossing of Mar Brava gametophytes from both species revealed that although it is rare, interfamilial hybridization between the two species is possible but mostly overcome by pseudogamy of female gametophytes.

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

“…Incomplete reproductive isolation between marine macrophytes has been widely reported in vitro from the congeneric to interfamilial level (Kraan & Guiry, 2000; Kraan et al, 2001; Druehl et al, 2005; Sanbonsuga & Neushul, 1978; Lewis & Neushul, 1995; Liptack & Druehl, 2000; Martins et al, 2019; Murúa et al, 2020; reviewed by Bartsch et al, 2008; Bolton, 2010). Even when hybridization is possible, reduced hybrid fitness can act as powerful filter maintaining species boundaries and genomic integrity.…”

Mates Matter: Gametophyte Kinship Recognition and Inbreeding in the Giant Kelp,Macrocystispyrifera(Laminariales, Phaeophyceae)

“…2019, Murúa et al. 2020), where the nucleus of the female gamete initiates a duplication of its genetic material without cell division, leading to the restoration of diploidy and the production of a juvenile sporophyte (e.g., Oppliger et al. 2007).…”

“…Models have predicted that a significant fraction (20-40%) of fertilization events in natural populations may be through selfing (Gaylord et al 2006, Johansson et al 2013. Unfertilized oogonia can also induce parthenogenesis, a common feature in kelps (Druehl et al 2005, Oppliger et al 2007, M€ uller et al 2019, Mur ua et al 2020, where the nucleus of the female gamete initiates a duplication of its genetic material without cell division, leading to the restoration of diploidy and the production of a juvenile sporophyte (e.g., Oppliger et al 2007). This reproductive system is expected to create fully homozygous individuals, therefore, representing the maximum level of inbreeding.…”

Individual Genetic Heterogeneity

“…An example is hybrid between gelada ( Theropithecus gelada ) and common baboon ( Papio hamadryas ), which interbreed occasionally in the wild [ 31 ]. Interfamilial hybrids are very rare; however, some instances are known, e.g., in kelps, brown algae seaweeds [ 32 ]. Hybridization has been used for development of novel species, especially in plant breeding to provide genetic variation and to improve properties [ 33 ].…”