The Evolution of Parasites From Their Hosts: A Case Study in the Parasitic Red Algae

Abstract

Abstract.-Morphological similarities of many parasites and their hosts have led to speculation that some groups of plant, animal, fungal, and algal parasites may have evolved directly from their hosts. These parasites, which have been termed adelphoparasites in the botanical literature, and more recently, agastoparasites in the insect literature, may evolve monophyletically from one host and radiate secondarily to other hosts or, these parasites may arise polyphyletically, each arising from its own host. In this study we compare the internal transcribed spacer regions of the nuclear ribosomal repeats of species and formae specialis (host races) included in the red algal parasite genus Asterocolax with its hosts, which all belong to the Phycodrys group of the Delesseriaceae and with closely related nonhost taxa of the Delesseriaceae. These analyses reveal that species of Asterocolax have evolved polyphyletically. Asterocolax erythroglossi from the North Atlantic host Erythroglossum laciniatum appears to have evolved from its host, whereas taxa included in the north Pacific species Asterocolax gardneri have had two independent origins. Asterocolax gardneri from the host Polyneura latissima probably arose directly from this host. In contrast, all other A. gardneri formae specialis appear to have originated from either Phycodrys setchellii or P. isabelliae and radiated secondarily onto other closely related taxa of the Phycodrys group, including Nienburgia andersoniana and Anisocladella pacifica. Gamete crossing experiments confirm that A. gardneri from each host is genetically isolated from both its host, and from other A. gardneri and their hosts. Cross-infection experiments reveal that A. gardneri develops normally only on its natural host, although some abberrant growth may occur on alternate hosts. The ability of red algal parasites to radiate secondarily to other red algal taxa, where they may become isolated genetically and speciate, suggests that this process of speciation is not a "genetic dead end" but one that may give rise to related clusters of parasite species.

Sympatric speciation through intraspecific social parasitism

“…This mode of radiation has been documented in various parasitic taxa, such as mistletoes (64), red algae (65), and gall wasps (66), and seems plausible also in bumblebee (35) and paper wasp inquilines (37). Alternatively, ''karavajevi'' may have increased its host array concurrently with speciation events in its original host lineage.…”

What's in a name? Monophyly of genera in the red algae: Rhodophyllis parasitica sp. nov. (Gigartinales, Rhodophyta); a new red algal parasite from New Zealand

“…Due to the morphological and genetic similarity of red algal parasite and host, it has been suggested that the parasite evolved from its host (Goff et al 1997, Blouin and Lane 2012, Ng et al 2013. For example, the parasite Congracilaria babae Yamamoto is more closely related to its host Gracilaria salicornia (C. Agardh) Dawson than the…”

“…Red algal parasites are common on other red algae and have been described from several orders within the Florideophyceae (Goff 1982), a few molecular-based phylogenetic studies have focused on a handful of species (Goff et al 1997, Zuccarello et al 2004, Ng et al 2013, with new species still being described (Kim and Cho 2010).…”

The evolution of parasites from their hosts: intra– and interspecific parasitism and Emery's rule

“…Ronquist 1994;Ward 1996;Lowe & Crozier 1997)). These phenomena are not conned to hymenopterans: Emery's rule also applies to groups of fungi, red algae and perhaps mistletoe (Goff et al (1997) and references therein). Three sequences of events have been suggested to lead to either strict or loose conformity with Emery's rule.…”