Expected and measured maximum diameter of protoconch I in planktotrophic sibling species after hypothetical additional cell cycles. Bold characters indicate concurrence between expected and measured protoconch I maximum diameter.
At least 10 pairs of similar, most probably closely related, species of Raphitoma are often sampled in the same Mediterranean localities. In each pair, one member bears a planktotrophic protoconch and the other a lecithotrophic one. We propose that the phenomenon may be attributed to a simple gene that functions in conjunction with others and environmental factors to exhibit a discontinuous multifactorial inheritance leading to poecilogony. Below a threshold, the animals may produce fewer and larger germ cells, giving rise to fewer and larger eggs and large lecithotrophic embryos with large paucispiral protoconch I, while above that threshold, more and smaller germ cells leading to smaller eggs and to planktotrophic larvae with small protoconch I and large multispiral protoconch II. Preliminary measurements are in support of our hypothesis. Analysis of mitochondrial DNA markers as well as interbreeding experiments could bring an end to the existing confusion.
- Mediterranean sea
Marine shelled gastropods follow, in general, three types of larval development: (1) direct, in which embryo development is completed in the egg capsule and the juvenile is ready to commence its benthic life immediately after hatching. (2) Lecithotrophic development in which, after hatching, the larva spends from a few minutes to several days as a veliger without feeding or growing. (3) Planktotrophic development, in which the larva hatches as a veliger and spends a few days to several months in the planktonic mode of life during which it feeds and grows . In all cases, a larval shell is formed which is called protoconch.
The size of fossilized early protoconches suggests that feeding (planktotrophic) embryos first appeared at the transition from the Cambrian era to the Ordovician as Ordovician protoconches were smaller than Cambrian ones indicating smaller Ordovician eggs and offspring. It is believed that planktotrophy would prolongate their escape from benthic predators and that an increasing nutrient supply and availability of photoautotrophic plankton in the world oceans of that period have facilitated both planktotrophy and suspension feeding . The eventual loss of planktotrophy in the Pliocene has been documented in some taxa of Conoidea (
Planktotrophic mode of life with long-living planktonic larvae is considered advantageous in the dispersal of the larvae as they may drift considerable distances with the currents [6, 7]. In addition, it has been demonstrated that the switch in some conoidean taxa from the planktotrophic to the non-planktotrophic development has increased their adaptive radiation, especially in polar or insular region, or in groups with narrow bathymetric distribution [3, 7]. In the case of
Within the Neogastropoda, Conoidea is a diverse superfamily of venomous and exclusively marine gastropods which harbors more than 300 genera, 4000 known species, and an estimated number of over 12,000 existing species [3, 12, 13]. Due to the species richness and the extensive homoplasy among shell’s features and the anterior alimentary system, they have resisted repeated attempts to be permanently classified with those attempts to be hindered primarily by the absence of a stable phylogenetic framework. Rather recently, DNA analysis provided an updated classification and divided the superfamily of Conoidea into 13 families [14–16]. Among them, the position of Raphitomidae is not sufficiently secured as a clade of Conoidea and for that reason there has been an on-going attempt to clarify the phylogeny of its Mediterranean members through a greater number of taxonomic data [17, 18]. These later publications have taken into account the pioneering works of Thorson [19, 20], concerning the relationship between the morphology of the protoconch and the type of the larval development in Caenogastropoda, e.g., the dichotomy “multispiral protoconch/planktotrophic development” and “paucispiral protoconch/lecithotrophic development” that has been widely accepted [6, 21]. Although some authors have used this dichotomy to divide species into planktotrophic genera and non-planktotrophic ones [3, 22, 23], it has been clearly demonstrated that such a division based exclusively on the morphology of the protoconch produces artificially separated polyphyletic taxa of otherwise distinct genera of closely related species. A separation, for instance, between the genus
Under the weight of the above unsettled situation, the aim of this study was to aid the classification of the Mediterranean
2. Materials and methods
Sampling of gastropods specimens was conducted from October 2008 to October 2016 in certain locations of Greece, according to Manousis and Galinou-Mitsoudi . The
The specimens are deposited in the premises of the Alexander Technological Educational Institute of Thessaloniki and those of Dr T. Manousis, Mr Constantinos Kontadakis, Mr George Mbazios and Mr Georgios Polyzoulis. Scientists are welcome to have access to the biological material at will.
Among the 570 specimens collected, three pairs of ‘sibling’ species of
It is generally accepted that the morphology of the gastropod protoconch determines the mode of development and the duration of larval stage in the ontogenesis [3, 6, 11]. We are of the opinion that such a change in the larval morphology in members of different genetically isolated molluscan lower taxa must have taken place independently and must be due to a simple genetic change involved in the cell’s contingency. Otherwise, it would be rather improbable for the same, yet complex, genetic changes to have taken place simultaneously in different individuals belonging to different taxa. Point mutations or even reverse mutations could easily occur leading also to switches. Such multiple switches in the mode of protoconch development are shown to have occurred in the evolutionary history of the Indo-Pacific
Both, planktotrophy and lecithotrophy commence with an initial short lecithotrophic stage equipped with the larval shell I. The initial difference between the two types of larval shells I lies in their size which, in turn, is associated with the size of the egg. Larval shell I, leading to multispiral protoconch II, is smaller in width and accounts for the planktotrophic developmental mode, whereas larval shell I, directly linked to lecithotrophy (paucispiral), is larger. In the case of the Mediterranean pair of the so-called sibling species,
|Pair of ‘sibling’ species||Measured lecithotrophic protoconch I maximum diameter (μm) (mean)||Expected planktotrophic protoconch I maximum diameter (μm) after one additional cell cycle||Expected planktotrophic protoconch I maximum diameter (μm) after two additional cell cycles||Expected planktrotophic protoconch I maximum diameter (μm) after three additional cell cycles||Measured planktotrophic protoconch I maximum diameter (μm) (mean)||Corresponding additional cell cycles|
Larger embryos (lecithotrophic) leave the water column early, while smaller ones (planktotrophic) later and thus continue with the development of protoconch II. In spite that time latency, both types of larvae eventually lose their buoyancy and sink. There seems to be no reason why, at least some of those two different types of larvae, not to find themselves in the same locality and, as the initial mutation responsible for the differentiation of the larval mode of life has not led to the establishment of a genetic barrier, when maturation is reached, to interbreed. There are no publications on interbreeding of Mediterranean ‘sibling’ species so that one can draw conclusions on the existence of a genetic barrier and thus to a confirmation that loss of either planktotrophy or lecithotrophy in the past has eventually led to speciation.
If there is no genetic barrier, then a rising question is associated with the type of inheritance imposed by the initial mutation on that gene controlling the germ cell cycle prior to meiosis. If it displayed a Mendelian inheritance, we would expect also the production of heterozygotes exhibiting a kind of semi-planktotrophic mode of life of shorter duration and presumably protoconches with fewer whorls. In conclusion, someone would expect to find in the same morphological species all three types of protoconches, e.g., paucispiral, multispiral, and intermediate. As this is not the case, at least in Mediterranean
In support to the above hypothesis, there are at least 10 pairs of similar, most probably closely related species of
Apart from the loss of planktotrophy (in our view, in some members of the same population, as mutations are random phenomena) in Raphitomidae, there is also a well-documented tendency for repeated loss of other conoidean important foregut structures such as radula, proboscis, and venom gland without alteration of the teleoconch morphology [12, 53–55]. Nevertheless, it is worth noting that the loss of planktotrophy in some turrids, like
Finally, through the present work the Raphitomid fauna of the Hellenic sea has been enriched by five new members as the search targeted appropriate environments such as biogenic backgrounds, maerl beds, and deeper waters.
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