Morhun H. Features of microevolution and adaptation in alien invertebrate species due to invasion into the Azov-Black Sea basin

Українська версія

Thesis for the degree of Doctor of Philosophy (PhD)

State registration number


Applicant for


  • 091 - Біологія. Біологія


Specialized Academic Board

ДФ 64.051.038

V.N. Karazin Kharkiv National University


This dissertation studies the invasions of invertebrate animals in water bodies of the Azov-Black Sea basin and specifies the features of microevolution in these populations as well as their phenotypic diversity. We studied the morphological variability of non-native populations, identified taxa by molecular marker cox1 (confirmed 47 native and 19 foreign taxa), and investigated the phylogenetic structure of several model species (leech Helobdella europaea, crustaceans Procambarus virginalis and Macrobrachium nipponense, mollusks Arcuatuala senhousia, Rapana venosa and Corbicula sp.). For two species (R. venosa and Corbicula sp.), we additionally applied multivariate statistical analysis of morphometric data. For 13 non-native species, DNA sequences were obtained firstly for populations from the Azov-Black Sea basin. Helobdella europaea and A. senhousia were recorded in the region for the first time. Procambarus virginalis and M. nipponense were recorded in new localities, indicating their range expansion. The phylogenetic analysis revealed an extremely low genetic diversity of H. europaea in the invasive regions throughout the world which is interpreted as a corroboration of the hypothesis of the introduction of this species from America (founder effect). The variability of the coloration pattern of longitudinal stripes was documented, which probably may be an adaptation to the color of substrates. Phylogenetic analysis of R. venosa demonstrated that the Odesa Bay’s population shared one haplotype, known from previous publications as the only one that occurs both in all invasion regions and native region. The conchological variability of rapa was analyzed using morphometric approach and differences in shell elongation were found. This tendencies in shape changes were attributed to the mollusk's adaptation to the substrate, in particular the need to hunt burrowing mollusks in the sand. No significant differences were found in the shape of shells between males and females, but males were larger. Also, it was demonstrated that the Black Sea population is smaller in size than the native ones and has a different sculpture and massiveness of the shells. The phylogenetic analysis of the parthenogenetic crayfish P. virginalis revealed the same haplotype in Dnipropetrovsk and Kharkiv regions, identical to all rest of crayfish from invasion regions, suggesting the founder effect. This species originated from the parental gonochronic P. fallax from the USA by autotriploidy during invasion. Compared to the parental species, P. virginalis, increased in size, became more fertile, and doubled its average lifespan. This is attributed to intensive DNA methylation. New localities and biotopes for the shrimp M. nipponense were found. The Chinese origin of the Dniester population was confirmed, and invasive history was revealed. The phylogenetic analysis found that there are different haplotypes in invasion regions. A new non-native bivalve in the region, A. senhousia, was recorded. The molecular analysis revealed two haplotypes with large large genetic distance between them. This is the result of the double uniparental mtDNA inheritance, which is specific to this species. The phylogenetic analysis involving sequences from previous studies showed that our sequence belongs to the cold-water clade. The formation of two clades (warm- and cold-water), revealed by Asif & Krug (2012), is thought to be preadaptation of these molluscs to the temperature. The phenotypic variability of coloration of A. senhousia clams was shown. Cytonuclear mismatches in Corbicula were found that resulted in the wrong morphotypes identification. The Ukrainian sample of Corbicula (morphotype R) from the Danube River shared the same haplotype with morphotypes Rlc and S. Was found that the Danubian Corbicula clams consisted of two different morphotypes. One of them is an unknown Corbicula sp., which is most probably of a hybrid origin between C. fluminalis and C. leana, since it has intermediate characters: sculpture of C. leana and hinge of C. fluminalis. Based on the molecular diversity and variability, the model species were classified in the context of the concept of Genetic Paradox of Biological Invasions (Estoup et al., 2016). The “genuine” paradox is characteristic to P. virginalis and Corbicula sp. which, although having extremely low genetic diversity, nevertheless demonstrate significant phenotypic variability. For H. europaea and R. venosa, it may be both a “genuine” and “spurious” paradox, since their cox1 haplotypes could have been selected due to selective pressure or preadaptation. There is no genetic paradox in M. nipponense invasions, as phylogenetic analysis indicates that several haplotypes occuring in different invasion regions. For A. senhousia, we also assume the absence of a paradox since there is a significant genetic diversity in the invasion regions and haplotypes which are now known only from the Ukrainian population.


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